[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.14348/molcells.2017.0115

Crosstalk and Interplay between the Ubiquitin-Proteasome System and Autophagy

Ji, Chang Hoon (Protein Metabolism Medical Research Center and Department of Biomedical Sciences, Seoul National University)
Kwon, Yong Tae (Protein Metabolism Medical Research Center and Department of Biomedical Sciences, Seoul National University)

Abstract

Proteolysis in eukaryotic cells is mainly mediated by the ubiquitin (Ub)-proteasome system (UPS) and the autophagy-lysosome system (hereafter autophagy). The UPS is a selective proteolytic system in which substrates are recognized and tagged with ubiquitin for processive degradation by the proteasome. Autophagy is a bulk degradative system that uses lysosomal hydrolases to degrade proteins as well as various other cellular constituents. Since the inception of their discoveries, the UPS and autophagy were thought to be independent of each other in components, action mechanisms, and substrate selectivity. Recent studies suggest that cells operate a single proteolytic network comprising of the UPS and autophagy that share notable similarity in many aspects and functionally cooperate with each other to maintain proteostasis. In this review, we discuss the mechanisms underlying the crosstalk and interplay between the UPS and autophagy, with an emphasis on substrate selectivity and compensatory regulation under cellular stresses.

Keywords

degradation signal (degron); macroautophagy; N-end rule pathway; N-terminal arginylation; proteolysis; protein quality control; ubiquitin code;

Citations & Related Records

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3	(2017) Cells The Role of Primary Cilia in the Crosstalk between the Ubiquitin–Proteasome System and Autophagy / 8 (3) , 241
4	(2019) Asian-Australasian journal of animal sciences Changes in expression of the autophagy-related genes microtubule-associated protein 1 light chain 3β and autophagy related 7 in skeletal muscle of fattening Japanese Black cattle: a pilot study / 32 (4) , 592
9	(2017) International journal of molecular sciences Cell Clearing Systems Bridging Neuro-Immunity and Synaptic Plasticity / 20 (9) , 2197
5	(2017) American journal of physiology. Cell physiology Protein arginylation of cytoskeletal proteins in the muscle: modifications modifying function / 316 (5) , C668
7	(2019) Cold Spring Harbor perspectives in biology Modulation of Amyloid States by Molecular Chaperones / 11 (7) , a033969
7	(2019) Phytopathology Ubiquitin Extension Protein UEP1 Modulates Cell Death and Resistance to Various Pathogens in Tobacco / 109 (7) , 1257
32	(2017) Proceedings of the National Academy of Sciences of the United States of America Gid10 as an alternative N-recognin of the Pro/N-degron pathway / 116 (32) , 15914
14	(2017) Journal of medicinal chemistry Proteasome Activation as a New Therapeutic Approach To Target Proteotoxic Disorders / 62 (14) , 6469
15	(2017) Molecules Proteasome Activation to Combat Proteotoxicity / 24 (15) , 2841
16	(2017) Aging Beta-amyloid induces apoptosis of neuronal cells by inhibition of the Arg/N-end rule pathway proteolytic activity / 11 (16) , 6134
10	(2019) Cells C9orf72 Proteins Regulate Autophagy and Undergo Autophagosomal or Proteasomal Degradation in a Cell Type-Dependent Manner / 8 (10) , 1233
11	(2017) Médecine sciences : M/S Autophagie et spermatozoïde / 35 (11) , 852
21	(2019) International journal of molecular sciences Juvenile Huntington’s Disease Skin Fibroblasts Respond with Elevated Parkin Level and Increased Proteasome Activity as a Potential Mechanism to Counterbalance the Pathological Consequences of Mu / 20 (21) , 5338
11	(2017) Toxins Ochratoxin A Sequentially Activates Autophagy and the Ubiquitin-Proteasome System / 11 (11) , 615
11	(2017) Biochemistry Ubiquitin Subproteome of Brain Mitochondria and Its Changes Induced by Experimental Parkinsonism and Action of Neuroprotectors / 84 (11) , 1359
1	(2019) Molecular cancer LncRNA LINRIS stabilizes IGF2BP2 and promotes the aerobic glycolysis in colorectal cancer / 18 (1) , 174
None	(2017) Frontiers in genetics Inhibition of Embryonic HSP 90 Function Promotes Variation of Cold Tolerance in Zebrafish / 11 (None) , 541944
None	(2017) Current medicinal chemistry The Role of Ubiquitin E3 Ligase in Atherosclerosis / 27 (None) , 152
None	(2017) eLife Parkin contributes to synaptic vesicle autophagy in Bassoon-deficient mice / 9 (None) , e56590
None	(2020) Frontiers in physiology Cardioprotective Role of Melatonin in Acute Myocardial Infarction / 11 (None) , 366
None	(2020) Frontiers in immunology KLICK Syndrome Linked to a <I>POMP</I> Mutation Has Features Suggestive of an Autoinflammatory Keratinization Disease / 11 (None) , 641
None	(2017) Frontiers in molecular biosciences FAIM Is a Non-redundant Defender of Cellular Viability in the Face of Heat and Oxidative Stress and Interferes With Accumulation of Stress-Induced Protein Aggregates / 7 (None) , 32
None	(2020) Frontiers in cell and developmental biology Multiple Functions of ATG8 Family Proteins in Plant Autophagy / 8 (None) , 466
2	(2017) American journal of physiology. Cell physiology Comment on “Everolimus induces G<SUB>1</SUB> cell cycle arrest through autophagy-mediated protein degradation of cyclin D1 in breast cancer cells” / 318 (2) , C448
4	(2017) Biochemistry Evolution of Substrates and Components of the Pro/N-Degron Pathway / 59 (4) , 582
4	(2017) Human & experimental toxicology The cytotoxic concentration of rosmarinic acid increases MG132-induced cytotoxicity, proteasome inhibition, autophagy, cellular stresses, and apoptosis in HepG2 cells / 39 (4) , 514
4	(2017) PLoS ONE Investigating AKT activation and autophagy in immunoproteasome-deficient retinal cells / 15 (4) , e0231212
9	(2017) Applied microbiology and biotechnology Rpn4 and proteasome-mediated yeast resistance to ethanol includes regulation of autophagy / 104 (9) , 4027
5	(2017) Cells Functional Characterisation of the Autophagy ATG12~5/16 Complex in <I>Dictyostelium discoideum</I> / 9 (5) , 1179
5	(2020) Oncology reports Transcriptome sequencing analysis of mono-ADP-ribosylation in colorectal cancer cells / 43 (5) , 1413
20	(2017) The Journal of biological chemistry High cell density increases glioblastoma cell viability under glucose deprivation via degradation of the cystine/glutamate transporter xCT (SLC7A11) / 295 (20) , 6936
10	(2017) Molecules Mechanisms Regulating the UPS-ALS Crosstalk: The Role of Proteaphagy / 25 (10) , 2352
20	(2017) Proceedings of the National Academy of Sciences of the United States of America Five enzymes of the Arg/N-degron pathway form a targeting complex: The concept of superchanneling / 117 (20) , 10778
25	(2017) Proceedings of the National Academy of Sciences of the United States of America Recognition of nonproline N-terminal residues by the Pro/N-degron pathway / 117 (25) , 14158
4	(2020) Medicinal research reviews How autophagy can restore proteostasis defects in multiple diseases? / 40 (4) , 1385
9	(2017) Cell death & disease <I>RNF115</I> deletion inhibits autophagosome maturation and growth of gastric cancer / 11 (9) , 810
3	(2020) The British journal of cancer CD133 inhibition via autophagic degradation in pemetrexed-resistant lung cancer cells by GMI, a fungal immunomodulatory protein from Ganoderma microsporum / 123 (3) , 449
30	(2017) Biochemistry The ATF3 Transcription Factor Is a Short-Lived Substrate of the Arg/N-Degron Pathway / 59 (30) , 2796
None	(2017) Mechanisms of ageing and development Nifedipine-induced AMPK activation alleviates senescence by increasing autophagy and suppressing of Ca<SUP>2+</SUP> levels in vascular smooth muscle cells / 190 (None) , 111314
9	(2020) Cells The Roles of Ubiquitin in Mediating Autophagy / 9 (9) , 2025
10	(2017) Cell death & disease RNF180 mediates STAT3 activity by regulating the expression of RhoC via the proteasomal pathway in gastric cancer cells / 11 (10) , 881
4	(2017) American journal of physiology, Endocrinology and metabolism IGF-1 inhibits MPTP/MPP<SUP>+</SUP>-induced autophagy on dopaminergic neurons through the IGF-1R/PI3K-Akt-mTOR pathway and GPER / 319 (4) , E734
11	(2017) Aging cell Autophagic receptor p62 protects against glycation‐derived toxicity and enhances viability / 19 (11) , e13257
4	(2020) Cancer and metastasis reviews Gastric cancer: a comprehensive review of current and future treatment strategies / 39 (4) , 1179
6	(2021) Journal of clinical rheumatology Exercise Training Attenuates Ubiquitin-Proteasome Pathway and Increases the Genes Related to Autophagy on the Skeletal Muscle of Patients With Inflammatory Myopathies / 27 (6) , S224
1	(2017) Cells Sorting Nexins in Protein Homeostasis / 10 (1) , 17
None	(2021) Frontiers in cell and developmental biology A Screen of Autophagy Compounds Implicates the Proteasome in Mammalian Aminoglycoside-Induced Hair Cell Damage / 9 (None) , 762751
None	(2017) Frontiers in pharmacology SC75741, A Novel c-Abl Inhibitor, Promotes the Clearance of TDP25 Aggregates via ATG5-Dependent Autophagy Pathway / 12 (None) , 741219
None	(2017) Biomedicine & pharmacotherapy Tumor Susceptibility Gene 101 facilitates rapamycin-induced autophagic flux in neuron cells / 134 (None) , 111106
4	(2017) International journal of molecular sciences The Autophagy Pathway: A Critical Route in the Disposal of Alpha 1-Antitrypsin Aggregates That Holds Many Mysteries / 22 (4) , 1875
None	(2017) Frontiers in molecular neuroscience Role of the Ubiquitin System in Chronic Pain / 14 (None) , 674914
4	(2017) Molecules Co-Chaperone Bag-1 Plays a Role in the Autophagy-Dependent Cell Survival through Beclin 1 Interaction / 26 (4) , 854
3	(2017) EMBO reports Biogenic amine neurotransmitters promote eicosanoid production and protein homeostasis / 22 (3) , None
8	(2017) ACS omega Toward Understanding the Biochemical Determinants of Protein Degradation Rates / 6 (8) , 5091
2	(2017) Biophysical reviews The dependency of autophagy and ubiquitin proteasome system during skeletal muscle atrophy / 13 (2) , 203
None	(2021) Neuroscience Switching the Proteolytic System from the Ubiquitin–Proteasome System to Autophagy in the Spinal Cord of an Amyotrophic Lateral Sclerosis Mouse Model / 466 (None) , 47
None	(2017) Tissue & cell Ubiquitin proteasome system and autophagy associated proteins in human testicular tumors / 71 (None) , 101513
8	(2021) Cells The Glyoxalase System in Age-Related Diseases: Nutritional Intervention as Anti-Ageing Strategy / 10 (8) , 1852
16	(2017) International journal of molecular sciences New Avenues for the Treatment of Huntington’s Disease / 22 (16) , 8363
16	(2021) International journal of molecular sciences Targeting Lysosomes to Reverse Hydroquinone-Induced Autophagy Defects and Oxidative Damage in Human Retinal Pigment Epithelial Cells / 22 (16) , 9042
9	(2021) Cells α-Synuclein Decreases the Abundance of Proteasome Subunits and Alters Ubiquitin Conjugates in Yeast / 10 (9) , 2229
6	(2017) Oncology reports Interactions between long non‑coding RNAs and RNA‑binding proteins in cancer (Review) / 46 (6) , 256
43	(2021) Proceedings of the National Academy of Sciences of the United States of America Aminopeptidases trim Xaa-Pro proteins, initiating their degradation by the Pro/N-degron pathway / 118 (43) , e2115430118
1	(2021) Nature communications VPS34 K29/K48 branched ubiquitination governed by UBE3C and TRABID regulates autophagy, proteostasis and liver metabolism / 12 (1) , 1322
11	(2017) The Plant cell The F-box E3 ubiquitin ligase BAF1 mediates the degradation of the brassinosteroid-activated transcription factor BES1 through selective autophagy in Arabidopsis / 33 (11) , 3532
21	(2021) Aging UBB+1 reduces amyloid-β cytotoxicity by activation of autophagy in yeast / 13 (21) , 23953
4	(2017) The EPMA journal Integrated genomic analysis of proteasome alterations across 11,057 patients with 33 cancer types: clinically relevant outcomes in framework of 3P medicine / 12 (4) , 605
12	(2021) Cells Overexpression of Neuroglobin Promotes Energy Metabolism and Autophagy Induction in Human Neuroblastoma SH-SY5Y Cells / 10 (12) , 3394
23	(2017) International journal of molecular sciences (20S) Ginsenoside Rh2 Exerts Its Anti-Tumor Effect by Disrupting the HSP90A-Cdc37 System in Human Liver Cancer Cells / 22 (23) , 13170
24	(2021) International journal of molecular sciences Interdependent Regulation of Polycystin Expression Influences Starvation-Induced Autophagy and Cell Death / 22 (24) , 13511
12	(2021) Autophagy CUL3 (cullin 3)-mediated ubiquitination and degradation of BECN1 (beclin 1) inhibit autophagy and promote tumor progression / 17 (12) , 4323
50	(2017) Proceedings of the National Academy of Sciences of the United States of America The N-terminal cysteine is a dual sensor of oxygen and oxidative stress / 118 (50) , e2107993118
1	(2022) Medical oncology AICAR enhances the cytotoxicity of PFKFB3 inhibitor in an AMPK signaling-independent manner in colorectal cancer cells / 39 (1) , 10
None	(2017) Neurotoxicology Ursolic acid ameliorates amyloid β-induced pathological symptoms in <I>Caenorhabditis elegans</I> by activating the proteasome / 88 (None) , 231
3	(2017) Biochimica et biophysica acta. Molecular basis of disease Hyperphosphatemia-induced degradation of transcription factor EB exacerbates vascular calcification / 1868 (3) , 166323