Proteome-wide identification of HSP70/HSC70 chaperone clients in human cells

PLoS Biology - Tập 18 Số 7 - Trang e3000606
Seung Woo Ryu1, Rose Stewart1, D. Chase Pectol2, Nicolette A. Ender1, Oshadi Wimalarathne1, Ji‐Hoon Lee1, Carlos Tadeu Pagani Zanini3, Antony Harvey4, Jon M. Huibregtse1, Peter Müeller3, Tanya T. Paull1
1The Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, United States of America
2The Department of Chemistry, Texas A&M University, College Station, Texas, United States of America
3Department of Statistics & Data Sciences, University of Texas at Austin, Austin, Texas, United States of America
4Thermo Fisher Scientific, Austin, Texas, United States of America

Tóm tắt

Từ khóa


Tài liệu tham khảo

P Sweeney, 2017, Protein misfolding in neurodegenerative diseases: implications and strategies, Transl Neurodegener, 6, 10.1186/s40035-017-0077-5

MS Hipp, 2014, Proteostasis impairment in protein-misfolding and -aggregation diseases, Trends Cell Biol, 24, 506, 10.1016/j.tcb.2014.05.003

FU Hartl, 2009, Converging concepts of protein folding in vitro and in vivo, Nat Struct Mol Biol, 16, 574, 10.1038/nsmb.1591

NB Nillegoda, 2018, Protein Disaggregation in Multicellular Organisms, Trends Biochem Sci, 43, 285, 10.1016/j.tibs.2018.02.003

MP Mayer, 2013, Hsp70 chaperone dynamics and molecular mechanism, Trends Biochem Sci, 38, 507, 10.1016/j.tibs.2013.08.001

A Finka, 2015, Multi-layered molecular mechanisms of polypeptide holding, unfolding and disaggregation by HSP70/HSP110 chaperones, Front Mol Biosci, 2, 10.3389/fmolb.2015.00029

E Meimaridou, 2008, From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery, J Mol Endocrinol, 42, 1, 10.1677/JME-08-0116

MR Fernández-Fernández, 2017, Hsp70—a master regulator in protein degradation, FEBS Lett, 591, 2648, 10.1002/1873-3468.12751

M Kabani, 2008, Multiple Hsp70 Isoforms in the Eukaryotic Cytosol: Mere Redundancy or Functional Specificity?, Curr Genomics, 9, 338, 10.2174/138920208785133280

M Daugaard, 2007, The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions, FEBS Lett, 581, 3702, 10.1016/j.febslet.2007.05.039

RP Beckmann, 1990, Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly, Science, 248, 850, 10.1126/science.2188360

J Frydman, 1996, Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms, Science, 272, 1497, 10.1126/science.272.5267.1497

V Albanèse, 2006, Systems Analyses Reveal Two Chaperone Networks with Distinct Functions in Eukaryotic Cells, Cell, 124, 75, 10.1016/j.cell.2005.11.039

R Shalgi, 2013, Widespread Regulation of Translation by Elongation Pausing in Heat Shock, Mol Cell, 49, 439, 10.1016/j.molcel.2012.11.028

CR Hunt, 2004, Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice, Mol Cell Biol, 24, 899, 10.1128/MCB.24.2.899-911.2004

Y Tutar, 2006, Primate chaperones Hsc70 (constitutive) and Hsp70 (induced) differ functionally in supporting growth and prion propagation in Saccharomyces cerevisiae, Genetics, 172, 851, 10.1534/genetics.105.048926

EM Clerico, 2015, How Hsp70 Molecular Machines Interact with Their Substrates to Mediate Diverse Physiological Functions, J Mol Biol, 427, 1575, 10.1016/j.jmb.2015.02.004

K Döring, 2017, Profiling Ssb-Nascent Chain Interactions Reveals Principles of Hsp70-, Assisted Folding. Cell, 170, 298

M Taipale, 2014, A quantitative chaperone interaction network reveals the architecture of cellular protein homeostasis pathways, Cell, 158, 434, 10.1016/j.cell.2014.05.039

AW Truman, 2015, Quantitative proteomics of the yeast Hsp70/Hsp90 interactomes during DNA damage reveal chaperone-dependent regulation of ribonucleotide reductase, J Proteomics, 112, 285, 10.1016/j.jprot.2014.09.028

Y Gong, 2009, An atlas of chaperone–protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell, Mol Syst Biol, 5, 10.1038/msb.2009.26

R Zhao, 2005, Navigating the Chaperone Network: An Integrative Map of Physical and Genetic Interactions Mediated by the Hsp90, Chaperone. Cell, 120, 715, 10.1016/j.cell.2004.12.024

M Taipale, 2012, Quantitative Analysis of Hsp90-Client Interactions Reveals Principles of Substrate Recognition, Cell, 150, 987, 10.1016/j.cell.2012.06.047

K Rizzolo, 2017, Features of the Chaperone Cellular Network Revealed through Systematic Interaction Mapping, Cell Rep, 20, 2735, 10.1016/j.celrep.2017.08.074

HF O’Connor, 2015, Ubiquitin-Activated Interaction Traps (UBAITs) identify E3 ligase binding partners, EMBO Rep, 16, 1699, 10.15252/embr.201540620

JA Ankney, 2018, Relative and Absolute Quantitation in Mass Spectrometry–Based Proteomics, Annu Rev Anal Chem, 11, 49, 10.1146/annurev-anchem-061516-045357

Yoav Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing, J R Stat Soc Ser B, 57, 289, 10.1111/j.2517-6161.1995.tb02031.x

W Kim, 2011, Systematic and Quantitative Assessment of the Ubiquitin-Modified Proteome, Mol Cell, 44, 325, 10.1016/j.molcel.2011.08.025

T Morán Luengo, 2018, Hsp90 Breaks the Deadlock of the Hsp70, Chaperone System. Mol Cell, 70, 545, 10.1016/j.molcel.2018.03.028

S Baindur-Hudson, 2015, The Networking of Chaperones by Co-chaperones, 69, 10.1007/978-3-319-11731-7_3

M Gebauer, 1997, Proteins interacting with the molecular chaperone hsp70/hsc70: physical associations and effects on refolding activity, FEBS Lett, 417, 109, 10.1016/S0014-5793(97)01267-2

A Bracher, 2015, GrpE, Hsp110/Grp170, HspBP1/Sil1 and BAG domain proteins: nucleotide exchange factors for Hsp70 molecular chaperones, Subcell Biochem, 78, 1, 10.1007/978-3-319-11731-7_1

J Radons, 2016, The human HSP70 family of chaperones: where do we stand?, Cell Stress Chaperones, 21, 379, 10.1007/s12192-016-0676-6

M Daugaard, 2007, The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions, FEBS Lett, 581, 3702, 10.1016/j.febslet.2007.05.039

V Chau, 1989, A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein, Science, 243, 1576, 10.1126/science.2538923

AA Glazier, 2018, HSC70 is a chaperone for wild-type and mutant cardiac myosin binding protein C, JCI Insigh, 3, 10.1172/jci.insight.99319

B Bercovich, 1997, Ubiquitin-dependent Degradation of Certain Protein Substrates in Vitro Requires the Molecular Chaperone Hsc70, J Biol Chem, 272, 9002, 10.1074/jbc.272.14.9002

MR Fernández-Fernández, 2017, Hsp70—a master regulator in protein degradation, FEBS Lett, 591, 2648, 10.1002/1873-3468.12751

MP Mayer, 2005, Hsp70 chaperones: cellular functions and molecular mechanism, Cell Mol Life Sci CMLS, 62, 670, 10.1007/s00018-004-4464-6

MP Mayer, 2000, Multistep mechanism of substrate binding determines chaperone activity of Hsp70, Nat Struct Biol, 7, 586, 10.1038/76819

A Ahmad, 2011, Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface, Proc Natl Acad Sci, 108, 18966, 10.1073/pnas.1111220108

A Brychzy, 2003, Cofactor Tpr2 combines two TPR domains and a J domain to regulate the Hsp70/Hsp90 chaperone system, EMBO J, 22, 3613, 10.1093/emboj/cdg362

HC Chang, 2004, The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila, J Cell Biol, 164, 1055, 10.1083/jcb.200311084

J Jiang, 2007, Structural basis of J cochaperone binding and regulation of Hsp70, Mol Cell, 28, 422, 10.1016/j.molcel.2007.08.022

MP Mayer, 2019, Recent advances in the structural and mechanistic aspects of Hsp70 molecular chaperones, J Biol Chem, 294, 2085, 10.1074/jbc.REV118.002810

A-M Fernandez-Escamilla, 2004, Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins, Nat Biotechnol, 22, 1302, 10.1038/nbt1012

S Maurer-Stroh, 2010, Exploring the sequence determinants of amyloid structure using position-specific scoring matrices, Nat Methods, 7, 237, 10.1038/nmeth.1432

KM Knee, 2013, Human TRiC complex purified from HeLa cells contains all eight CCT subunits and is active in vitro, Cell Stress Chaperones, 18, 137, 10.1007/s12192-012-0357-z

VA Lewis, 1992, T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol, Nature, 358, 249, 10.1038/358249a0

J Cuéllar, 2008, The structure of CCT-Hsc70 NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin, Nat Struct Mol Biol, 15, 858, 10.1038/nsmb.1464

AM Cuervo, 2014, Chaperone-mediated autophagy: roles in disease and aging, Cell Res, 24, 92, 10.1038/cr.2013.153

IR Taylor, 2018, The disorderly conduct of Hsc70 and its interaction with the Alzheimer’s-related Tau protein, J Biol Chem, 293, 10796, 10.1074/jbc.RA118.002234

S Kaushik, 2015, Degradation of lipid droplet-associated proteins by chaperone-mediated autophagy facilitates lipolysis, Nat Cell Biol, 17, 759, 10.1038/ncb3166

OR Brekk, 2019, Impairment of chaperone-mediated autophagy affects neuronal homeostasis through altered expression of DJ-1 and CRMP-2 proteins, Mol Cell Neurosci, 95, 1, 10.1016/j.mcn.2018.12.006

M Pajares, 2018, Transcription factor NFE2L2/NRF2 modulates chaperone-mediated autophagy through the regulation of LAMP2A, Autophagy, 14, 1310, 10.1080/15548627.2018.1474992

L Liu, 2018, Ac2-26 Induces IKKβ Degradation Through Chaperone-Mediated Autophagy Via HSPB1 in NCM-Treated Microglia, Front Mol Neurosci, 11, 76, 10.3389/fnmol.2018.00076

Y Liu, 2016, EF1A1/HSC70 Cooperatively Suppress Brain Endothelial Cell Apoptosis via Regulating JNK Activity, CNS Neurosci Ther, 22, 836, 10.1111/cns.12581

H Saitoh, 1995, The RCC1 protein interacts with Ran, RanBP1, hsc70, and a 340-kDa protein in Xenopus extracts, J Biol Chem, 270, 10658, 10.1074/jbc.270.18.10658

I Hwang, 2018, Chaperone-E3 Ligase Complex HSP70-CHIP Mediates Ubiquitination of Ribosomal Protein S3, Int J Mol Sci, 19, 10.3390/ijms19092723

D Tang, 2007, Nuclear heat shock protein 72 as a negative regulator of oxidative stress (hydrogen peroxide)-induced HMGB1 cytoplasmic translocation and release, J Immunol Baltim Md, 178, 7376

IV Guzhova, 2011, Novel mechanism of Hsp70 chaperone-mediated prevention of polyglutamine aggregates in a cellular model of huntington disease, Hum Mol Genet, 20, 3953, 10.1093/hmg/ddr314

H Matsui, 2019, Identification of a Promiscuous Epitope Peptide Derived From HSP70, J Immunother Hagerstown Md 1997, 42, 244

B Xhabija, 2015, Receptor-mediated Endocytosis 8 Utilizes an N-terminal Phosphoinositide-binding Motif to Regulate Endosomal Clathrin Dynamics, J Biol Chem, 290, 21676, 10.1074/jbc.M115.644757

T Johansson, 2004, Detection of binding partners to the profilin:actin complex by far Western and mass spectrometry analyses, Anal Biochem, 335, 228, 10.1016/j.ab.2004.09.006

L Zhang, 2013, Requirement of heat shock protein 70 for inducible nitric oxide synthase induction, Cell Signal, 25, 1310, 10.1016/j.cellsig.2013.02.004

JY Kim, 2015, Regulation of inflammatory transcription factors by heat shock protein 70 in primary cultured astrocytes exposed to oxygen-glucose deprivation, Neuroscience, 286, 272, 10.1016/j.neuroscience.2014.11.057

G Hiyama, 2014, Sperm activation by heat shock protein 70 supports the migration of sperm released from sperm storage tubules in Japanese quail (Coturnix japonica), Reprod Camb Engl, 147, 167, 10.1530/REP-13-0439

M Moghanibashi, 2013, Esophageal cancer alters the expression of nuclear pore complex binding protein Hsc70 and eIF5A-1, Funct Integr Genomics, 13, 253, 10.1007/s10142-013-0320-9

KJ Roux, 2018, BioID: A Screen for Protein‐Protein Interactions. Curr Protoc Protein Sci, 91

DI Kim, 2016, An improved smaller biotin ligase for BioID proximity labeling. Zheng Y, editor, Mol Biol Cell, 27, 1188, 10.1091/mbc.E15-12-0844

F Willmund, 2013, The Cotranslational Function of Ribosome-Associated Hsp70 in Eukaryotic Protein Homeostasis, Cell, 152, 196, 10.1016/j.cell.2012.12.001

A Shiber, 2018, Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling, Nature, 561, 268, 10.1038/s41586-018-0462-y

AJ McClellan, 2005, Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways, Cell, 121, 739, 10.1016/j.cell.2005.03.024

S-H Park, 2007, The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome system, Mol Biol Cell, 18, 153, 10.1091/mbc.e06-04-0338

V Arndt, 2007, To be, or not to be—molecular chaperones in protein degradation, Cell Mol Life Sci CMLS, 64, 2525, 10.1007/s00018-007-7188-6

I Kamenova, 2019, Co-translational assembly of mammalian nuclear multisubunit complexes, Nat Commun, 10, 1740, 10.1038/s41467-019-09749-y

GS Stewart, 1999, The DNA double-strand break repair gene hMre11 is mutated in individuals with an Ataxia-Telangiectasia-like disorder, Cell, 99, 577, 10.1016/S0092-8674(00)81547-0

DC Chow, 1995, Functional significance of the beta-subunit for heterodimeric P-type ATPases, J Exp Biol, 198, 1, 10.1242/jeb.198.1.1

MA Edelbrock, 2013, Structural, molecular and cellular functions of MSH2 and MSH6 during DNA mismatch repair, damage signaling and other noncanonical activities, Mutat Res, 743–744, 53, 10.1016/j.mrfmmm.2012.12.008

M Bourdenx, 2017, Protein aggregation and neurodegeneration in prototypical neurodegenerative diseases: Examples of amyloidopathies, tauopathies and synucleinopathies, Prog Neurobiol, 155, 171, 10.1016/j.pneurobio.2015.07.003

P Sweeney, 2017, Protein misfolding in neurodegenerative diseases: implications and strategies, Transl Neurodegener, 6, 10.1186/s40035-017-0077-5

P Corcia, 2017, Genetics of amyotrophic lateral sclerosis, Rev Neurol (Paris), 173, 254, 10.1016/j.neurol.2017.03.030

RL Redler, 2014, Non-native Soluble Oligomers of Cu/Zn Superoxide Dismutase (SOD1) Contain a Conformational Epitope Linked to Cytotoxicity in Amyotrophic Lateral Sclerosis (ALS), Biochemistry, 53, 2423, 10.1021/bi500158w

J-H Lee, 2018, ATM directs DNA damage responses and proteostasis via genetically separable pathways, Sci Signal, 11

HF O’Connor, 2015, Ubiquitin-Activated Interaction Traps (UBAITs) identify E3 ligase binding partners, EMBO Rep, 16, 1699, 10.15252/embr.201540620

HF O’Connor, 2018, The Ubiquitin Proteasome System, 85, 10.1007/978-1-4939-8706-1_7

B Meyer, 2011, 100% protein sequence coverage: a modern form of surrealism in proteomics, Amino Acids, 41, 291, 10.1007/s00726-010-0680-6

J Hageman, 2009, Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library, Cell Stress Chaperones, 14, 1, 10.1007/s12192-008-0060-2

NE Sanjana, 2014, Improved vectors and genome-wide libraries for CRISPR screening, Nat Methods, 11, 783, 10.1038/nmeth.3047

FS Leach, 1993, Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer, Cell, 75, 1215, 10.1016/0092-8674(93)90330-S

H Jaiswal, 2011, The chaperone network connected to human ribosome-associated complex, Mol Cell Biol, 31, 1160, 10.1128/MCB.00986-10

JH Lee, 2006, Purification and biochemical characterization of ataxia-telangiectasia mutated and Mre11/Rad50/Nbs1, Methods Enzym, 408, 529, 10.1016/S0076-6879(06)08033-5