29,147
Views
88
CrossRef citations to date
0
Altmetric
Review

Mitophagy in degenerative joint diseases

, , , &
Pages 2082-2092 | Received 22 May 2020, Accepted 04 Sep 2020, Published online: 24 Sep 2020

References

  • Vergroesen PPA, Kingma I, Emanuel KS, et al. Mechanics and biology in intervertebral disc degeneration: a vicious circle. Osteoarthr Cartilage. 2015;23:1057–1070.
  • Risbud MV, Schoepflin ZR, Mwale F, et al. Defining the phenotype of young healthy nucleus pulposus cells: recommendations of the Spine Research Interest Group at the 2014 annual ORS meeting. J Orthop Res. 2015;33:283–293.
  • Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function. Sports Health. 2009;1:461–468.
  • Deng ZH, Li YS, Gao X, et al. Bone morphogenetic proteins for articular cartilage regeneration. Osteoarthr Cartilage. 2018;26:1153–1161.
  • Adams MA, Roughley PJ. What is Intervertebral Disc Degeneration, and What Causes It? Spine (Phila Pa 1976). 2006;31(18):2151–2161.
  • Rahmati M, Nalesso G, Mobasheri A, et al. Aging and osteoarthritis: central role of the extracellular matrix. 2017;20–30.
  • Maher C, Underwood M, Buchbinder R. Non-specific low back pain. Lancet. 2017;389:736–747.
  • Hunter DJ, Bierma-Zeinstra S. Osteoarthritis. Lancet. 2019;393:1745–1759.
  • Loeser RF, Collins JA, Diekman BO. Ageing and the pathogenesis of osteoarthritis. Nat Rev Rheumatol. 2016;12:412–420.
  • Wu PH, Kim HS, Jang I. Intervertebral disc diseases PART 2: a review of the current diagnostic and treatment strategies for intervertebral disc disease. 202021(6):2135.
  • Wallace DC. A mitochondrial bioenergetic etiology of disease. J Clin Invest. 2013;123:1405–1412.
  • Giorgi C, Marchi S, Simoes ICM, et al. Mitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases. Int Rev Cell Mol Biol. 2018;340:209–344.
  • Palikaras K, Lionaki E, Tavernarakis N. Mechanisms of mitophagy in cellular homeostasis, physiology and pathology. Nat Cell Biol. 2018;20:1013–1022.
  • Esteban-Martínez L, Boya P. BNIP3L/NIX-dependent mitophagy regulates cell differentiation via metabolic reprogramming. AUTOPHAGY. 2018;14:915–917.
  • Peña-Blanco A, Haschka MD, Jenner A, et al. Drp1 modulates mitochondrial stress responses to mitotic arrest. Cell Death Differ. 2020;27(9):2620–2634.
  • Shaltouki A, Hsieh C, Kim MJ, et al. Alpha-synuclein delays mitophagy and targeting Miro rescues neuron loss in Parkinson’s models. ACTA NEUROPATHOL. 2018;136:607–620.
  • Zhang Z, Xu T, Chen J, et al. Parkin-mediated mitophagy as a potential therapeutic target for intervertebral disc degeneration. Cell Death Dis. 2018;9:980.
  • Ansari MY, Khan NM, Ahmad I, et al. Parkin clearance of dysfunctional mitochondria regulates ROS levels and increases survival of human chondrocytes. Osteoarthr Cartilage. 2018;26(8):1087–1097.
  • Chen G, Kroemer G, Kepp O. Mitophagy: an emerging role in aging and age-associated diseases. Front Cell Dev Biol. 2020;8:200.
  • Clark IE, Dodson MW, Jiang C, et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. NATURE. 2006;441:1162–1166.
  • Pickles S, Vigié P, Youle RJ. Mitophagy and quality control mechanisms in mitochondrial maintenance. Curr Biol. 2018;28:R170–R185.
  • Harper JW, Ordureau A, Heo J. Building and decoding ubiquitin chains for mitophagy. Nat Rev Mol Cell Bio. 2018;19:93–108.
  • Jin SM, Lazarou M, Wang C, et al. Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J Cell Biol. 2010;191:933–942.
  • Meer C, Lorenz H, Weihofen A, et al. The mitochonrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking. J Neurochem. 2011;117:856–867.
  • Yamano K, Youle RJ. PINK1 is degraded through the N-end rule pathway. AUTOPHAGY. 2013;9:1758–1769.
  • Kondapalli C, Kazlauskaite A, Zhang N, et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol. 2012;2:120080.
  • Shiba-Fukushima K, Imai Y, Yoshida S, et al. PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep-uk. 2012;2:1002.
  • Ordureau A, Sarraf SA, Duda DM, et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol Cell. 2014;56:360–375.
  • Koyano F, Okatsu K, Kosako H, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 2014;510:162–166.
  • Aguirre JD, Dunkerley KM, Mercier P, et al. Structure of phosphorylated UBL domain and insights into PINK1-orchestrated parkin activation. Proc Natl Acad Sci U S A. 2017;114:298–303.
  • Bingol B, Tea JS, Phu L, et al. The mitochondrial deubiquitinase USP30 opposes parkin-mediated mitophagy. NATURE. 2014;510:370–375.
  • Wang Y, Serricchio M, Jauregui M, et al. Deubiquitinating enzymes regulate PARK2-mediated mitophagy. AUTOPHAGY. 2015;11:595–606.
  • Cornelissen T, Haddad D, Wauters F, et al. The deubiquitinase USP15 antagonizes Parkin-mediated mitochondrial ubiquitination and mitophagy. Hum Mol Genet. 2014;23:5227–5242.
  • Tanaka A, Cleland MM, Xu S, et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol. 2010;191:1367–1380.
  • Safiulina D, Kuum M, Choubey V, et al. Miro proteins prime mitochondria for Parkin translocation and mitophagy. Embo J. 2019;38:e99384.
  • Shlevkov E, Kramer T, Schapansky J, et al. Miro phosphorylation sites regulate Parkin recruitment and mitochondrial motility. Proc Natl Acad Sci U S A. 2016;113:E6097–E6106.
  • Sun Y, Vashisht AA, Tchieu J, et al. Voltage-dependent anion channels (VDACs) recruit Parkin to defective mitochondria to promote mitochondrial autophagy. J Biol Chem. 2012;287:40652–40660.
  • Bernardini JP, Brouwer JM, Tan IK, et al. Parkin inhibits BAK and BAX apoptotic function by distinct mechanisms during mitophagy. Embo J. 2019;38:e99916.
  • Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. NATURE. 2015;524:309–314.
  • Wong YC, Holzbaur ELF. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A. 2014;111:E4439–E4448.
  • Geisler S, Holmström KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol. 2010;12:119–131.
  • Narendra D, Tanaka A, Suen D, et al. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol. 2008;183:795–803.
  • Li X, He S, Ma B. Autophagy and autophagy-related proteins in cancer. Mol Cancer. 2020;19:12.
  • Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283:10892–10903.
  • Sowter HM, Ratcliffe PJ, Watson P, et al. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 2001;61:6669.
  • Dhingra R, Gang H, Wang Y, et al. Bidirectional regulation of nuclear factor-κB and mammalian target of rapamycin signaling functionally links bnip3 gene repression and cell survival of ventricular myocytes. Circulation. 2013;6:335–343.
  • Chaanine AH, Kohlbrenner E, Gamb SI, et al. FOXO3a regulates BNIP3 and modulates mitochondrial calcium, dynamics, and function in cardiac stress. Am J Physiol Heart Circ Physiol. 2016;311:H1540–H1559.
  • Nakamura Y, Kitamura N, Shinogi D, et al. BNIP3 and NIX mediate Mieap-induced accumulation of lysosomal proteins within mitochondria. Plos One. 2012;7:e30767.
  • Gugnoni M, Sancisi V, Gandolfi G, et al. Cadherin-6 promotes EMT and cancer metastasis by restraining autophagy. ONCOGENE. 2017;36:667–677.
  • Novak I, Kirkin V, McEwan DG, et al. Nix is a selective autophagy receptor for mitochondrial clearance. Embo Rep. 2010;11:45–51.
  • Aerbajinai W, Giattina M, Lee YT, et al. The proapoptotic factor Nix is coexpressed with Bcl-xL during terminal erythroid differentiation. BLOOD. 2003;102:712–717.
  • Schweers RL, Zhang J, Randall MS, et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A. 2007;104:19500–19505.
  • Chen M, Chen Z, Wang Y, et al. Mitophagy receptor FUNDC1 regulates mitochondrial dynamics and mitophagy. AUTOPHAGY. 2016;12:689–702.
  • Wu W, Tian W, Hu Z, et al. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. Embo Rep. 2014;15:566–575.
  • Chen G, Han Z, Feng D, et al. A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol Cell. 2014;54:362–377.
  • Wu W, Lin C, Wu K, et al. FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions. Embo J. 2016;35:1368–1384.
  • Strappazzon F, Nazio F, Corrado M, et al. AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1. Cell Death Differ. 2015;22:419–432.
  • Chu CT, Ji J, Dagda RK, et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol. 2013;15:1197–1205.
  • Sentelle RD, Senkal CE, Jiang W, et al. Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat Chem Biol. 2012;8:831–838.
  • Williams FMK, Bansal AT, van Meurs JB, et al. Novel genetic variants associated with lumbar disc degeneration in northern Europeans: a meta-analysis of 4600 subjects. Ann Rheum Dis. 2013;72:1141–1148.
  • Feng C, Yang M, Lan M, et al. ROS: crucial intermediators in the pathogenesis of intervertebral disc degeneration. Oxid Med Cell Longev. 2017;2017:5601593.
  • Xu W, Zheng H, Yang R, et al. Mitochondrial NDUFA4L2 attenuates the apoptosis of nucleus pulposus cells induced by oxidative stress via the inhibition of mitophagy. Exp Mol Med. 2019;51:1–16.
  • Wang Y, Shen J, Chen Y, et al. PINK1 protects against oxidative stress induced senescence of human nucleus pulposus cells via regulating mitophagy. Biochem Biophys Res Commun. 2018;504:406–414.
  • Kang L, Liu S, Li J, et al. Parkin and Nrf2 prevent oxidative stress-induced apoptosis in intervertebral endplate chondrocytes via inducing mitophagy and anti-oxidant defenses. Life Sci. 2020;243:117244.
  • Liesa M, Shirihai OS. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013;17:491–506.
  • Chen Y, Lin J, Chen J, et al. Mfn2 is involved in intervertebral disc degeneration through autophagy modulation. Osteoarthr Cartilage. 2020;28:363–374.
  • Kristensen LS, Andersen MS, Stagsted LVW, et al. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20:675–691.
  • Xie L, Huang W, Fang Z, et al. CircERCC2 ameliorated intervertebral disc degeneration by regulating mitophagy and apoptosis through miR-182-5p/SIRT1 axis. Cell Death Dis. 2019;10:751.
  • Cipolla-Neto J, Amaral FGD. Melatonin as a Hormone: new Physiological and Clinical Insights. Endocr Rev. 2018;39:990–1028.
  • Kang J, Hong J, Lee S. Melatonin enhances mitophagy and mitochondrial biogenesis in rats with carbon tetrachloride-induced liver fibrosis. J Pineal Res. 2016;60:383–393.
  • Lee JH, Yoon YM, Song K, et al. Melatonin suppresses senescence-derived mitochondrial dysfunction in mesenchymal stem cells via the HSPA1L-mitophagy pathway. Aging Cell. 2020;19:e13111.
  • Chen Y, Wu Y, Shi H, et al. Melatonin ameliorates intervertebral disc degeneration via the potential mechanisms of mitophagy induction and apoptosis inhibition. J Cell Mol Med. 2019;23:2136–2148.
  • Cerdá B, Periago P, Espín JC, et al. Identification of Urolithin A as a Metabolite Produced by Human Colon Microflora from Ellagic Acid and Related Compounds. J Agr Food Chem. 2005;53:5571–5576.
  • Lin J, Zhuge J, Zheng X, et al. Urolithin A-induced mitophagy suppresses apoptosis and attenuates intervertebral disc degeneration via the AMPK signaling pathway. Free Radical Bio Med. 2020;150:109–119.
  • Pillai VB, Samant S, Sundaresan NR, et al. Honokiol blocks and reverses cardiac hypertrophy in mice by activating mitochondrial Sirt3. Nat Commun. 2015;6:6656.
  • Wang J, Nisar M, Huang C, et al. Small molecule natural compound agonist of SIRT3 as a therapeutic target for the treatment of intervertebral disc degeneration. Exp Mol Med. 2018;50:1–14.
  • Huang D, Peng Y, Li Z, et al. Compression-induced senescence of nucleus pulposus cells by promoting mitophagy activation via the PINK1/PARKIN pathway. J Cell Mol Med. 2020;24:5850–5864.
  • Ni H, Williams JA, Ding W. Mitochondrial dynamics and mitochondrial quality control. Redox Biol. 2015;4:6–13.
  • Kang L, Liu S, Li J, et al. The mitochondria-targeted anti-oxidant MitoQ protects against intervertebral disc degeneration by ameliorating mitochondrial dysfunction and redox imbalance. Cell Proliferat. 2020;53:e12779.
  • Liu J, Wang J, Zhou Y. Upregulation of BNIP3 and translocation to mitochondria in nutrition deprivation induced apoptosis in nucleus pulposus cells. Joint Bone Spine. 2012;79:186–191.
  • Liu J, Yuan C, Pu L, et al. Nutrient deprivation induces apoptosis of nucleus pulposus cells via activation of the BNIP3/AIF signalling pathway. Mol Med Rep. 2017;16:7253–7260.
  • He Z, Pu L, Yuan C, et al. Nutrition deficiency promotes apoptosis of cartilage endplate stem cells in a caspase-independent manner partially through upregulating BNIP3. Acta Bioch Bioph Sin. 2017;49:25–32.
  • Lomonosova E, Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. ONCOGENE. 2008;27(Suppl 1):S2–S19.
  • Jin Q, Li R, Hu N, et al. DUSP1 alleviates cardiac ischemia/reperfusion injury by suppressing the Mff-required mitochondrial fission and Bnip3-related mitophagy via the JNK pathways. Redox Biol. 2018;14:576–587.
  • Webb AE, Brunet A. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci. 2014;39:159–169.
  • Wang Y, Yang Y, Zuo R, et al. FOXO3 protects nucleus pulposus cells against apoptosis under nutrient deficiency via autophagy. Biochem Biophys Res Commun. 2020;524:756–763.
  • Xu W, Yang R, Zheng H, et al. PGC-1α acts as an mediator of Sirtuin2 to protect annulus fibrosus from apoptosis induced by oxidative stress through restraining mitophagy. Int J Biol Macromol. 2019;136:1007–1017.
  • Shin HJ, Park H, Shin N, et al. Pink1-Mediated Chondrocytic Mitophagy Contributes to Cartilage Degeneration in Osteoarthritis. J Clin Med. 2019;8:1849.
  • Kapoor M, Martel-Pelletier J, Lajeunesse D, et al. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol. 2010;7:33.
  • Wang C, Yang Y, Zhang Y, et al. Protective effects of metformin against osteoarthritis through upregulation of SIRT3-mediated PINK1/Parkin-dependent mitophagy in primary chondrocytes. Biosci Trends. 2018;12:605–612.
  • Maimaitijuma T, Yu J, Ren Y, et al. PHF23 negatively regulates the autophagy of chondrocytes in osteoarthritis. Life Sci. 2020;253:117750.
  • D’Adamo S, Cetrullo S, Guidotti S, et al. Spermidine rescues the deregulated autophagic response to oxidative stress of osteoarthritic chondrocytes. Free Radical Bio Med. 2020;153:159–172.
  • Hosseinpour-Moghaddam K, Caraglia M, Sahebkar A. Autophagy induction by trehalose: molecular mechanisms and therapeutic impacts. J Cell Physiol. 2018;233:6524–6543.
  • Tang Q, Zheng G, Feng Z, et al. Trehalose ameliorates oxidative stress-mediated mitochondrial dysfunction and ER stress via selective autophagy stimulation and autophagic flux restoration in osteoarthritis development. Cell Death Dis. 2017;8:e3081.
  • Corciulo C, Lendhey M, Wilder T, et al. Endogenous adenosine maintains cartilage homeostasis and exogenous adenosine inhibits osteoarthritis progression. Nat Commun. 2017;8:15019.
  • Castro CM, Corciulo C, Solesio ME, et al. Adenosine A2A receptor (A2AR) stimulation enhances mitochondrial metabolism and mitigates reactive oxygen species-mediated mitochondrial injury. FASEB J. 2020;34:5027–5045.
  • Rustenburg CME, Emanuel KS, Peeters M, et al. Osteoarthritis and intervertebral disc degeneration: quite different, quite similar. JOR spine. 2018;1:e1033.
  • Ryu D, Mouchiroud L, Andreux PA, et al. Urolithin A induces mitophagy and prolongs lifespan in C. elegans and increases muscle function in rodents. Nat Med. 2016;22:879–888.
  • Fitzsimmons REB, Mazurek MS, Soos A, et al. Mesenchymal stromal/stem cells in regenerative medicine and tissue engineering. Stem Cells Int. 2018;2018:8031718.
  • Mazzotti E, Teti G, Falconi M, et al. Age-Related Alterations Affecting the Chondrogenic Differentiation of Synovial Fluid Mesenchymal Stromal Cells in an Equine Model. CELLS-BASEL. 2019;8:1116.
  • Fan P, Yu X, Xie X, et al. Mitophagy is a protective response against oxidative damage in bone marrow mesenchymal stem cells. Life Sci. 2019;229:36–45.
  • Fang EF, Hou Y, Palikaras K, et al. Mitophagy inhibits amyloid-β and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease. Nat Neurosci. 2019;22:401–412.
  • Madeo F, Eisenberg T, Pietrocola F, et al. Spermidine in health and disease. SCIENCE. 2018;359:n2788.
  • Wang H, Jiang T, Li W, et al. Resveratrol attenuates oxidative damage through activating mitophagy in an in vitro model of Alzheimer’s disease. Toxicol Lett. 2018;282:100–108.
  • Bakula D, Scheibye-Knudsen M. MitophAging: mitophagy in Aging and Disease. Front Cell Dev Biol. 2020;8:239.
  • Dodson MW, Guo M. Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson’s disease. Curr Opin Neurobiol. 2007;17:331–337.
  • Irrcher I, Aleyasin H, Seifert EL, et al. Loss of the Parkinson’s disease-linked gene DJ-1 perturbs mitochondrial dynamics. Hum Mol Genet. 2010;19:3734–3746.
  • Bravo-San PJM, Kroemer G, Galluzzi L. Autophagy and mitophagy in cardiovascular disease. Circ Res. 2017;120:1812–1824.