Advanced search
Publication Cover
Autophagy Volume 15, 2019 - Issue 9
Submit an article Journal homepage
17,976
Views
77
CrossRef citations to date
0
Altmetric
Research Paper

Mitochondrial respiratory chain deficiency inhibits lysosomal hydrolysis

Lorena Fernandez-MosqueraInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, Germany;Doctoral Program in Molecular Medicine, Georg August University Goettingen, Goettingen, GermanyORCID Iconhttps://orcid.org/0000-0003-4606-5056View further author information
ORCID Icon,
King Faisal YambireInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, Germany;International Max-Planck Research School in Neuroscience, Goettingen, Germany;European Neuroscience Institute Goettingen, University Medical Center Goettingen and Max-Planck Society, Goettingen, GermanyORCID Iconhttps://orcid.org/0000-0003-2417-450XView further author information
ORCID Icon,
Renata CoutoInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, Germany;Doctoral Program in Molecular Biology of Cells, Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences, University of Goettingen, Goettingen, GermanyView further author information
,
Leonardo PereyraInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, Germany;Doctoral Program in Molecular Biology of Cells, Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences, University of Goettingen, Goettingen, GermanyORCID Iconhttps://orcid.org/0000-0002-9139-9664View further author information
ORCID Icon,
Kamil PabisInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, GermanyORCID Iconhttps://orcid.org/0000-0002-1120-3079View further author information
ORCID Icon,
Amy H. PonsfordInstitute of Translational Medicine, University of Liverpool, Liverpool, UKView further author information
,
Cátia V. DiogoInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, GermanyView further author information
,
Massimiliano StagiInstitute of Translational Medicine, University of Liverpool, Liverpool, UKORCID Iconhttps://orcid.org/0000-0002-5827-902XView further author information
ORCID Icon,
Ira MilosevicEuropean Neuroscience Institute Goettingen, University Medical Center Goettingen and Max-Planck Society, Goettingen, GermanyORCID Iconhttps://orcid.org/0000-0001-6440-3763View further author information
ORCID Icon &
Nuno RaimundoInstitute of Cellular Biochemistry, University Medical Center Goettingen, Goettingen, GermanyCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-5988-9129View further author information
ORCID Icon show all
Pages 1572-1591 | Received 30 Mar 2018, Accepted 11 Feb 2019, Published online: 27 Mar 2019

References

  • McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol. 2006 Jul 25;16(14):R551–60. . PubMed PMID: 16860735; eng.
  • Kasahara A, Scorrano L. Mitochondria: from cell death executioners to regulators of cell differentiation. Trends Cell Biol. 2014 Dec;24(12):761–770. PubMed PMID: 25189346; eng.
  • Raimundo N, Mosquera LF, Yambire KF. Mitochondrial Signaling. In: Hockenberry DM, editor. Mitochondria and cell death. Springer; 2015. p. 169–184.
  • Raimundo N. Mitochondrial pathology: stress signals from the energy factory. Trends Mol Med. 2014 May;20(5):282–292. PubMed PMID: 24508276; eng.
  • Bento CF, Renna M, Ghislat G, et al. Mammalian autophagy: how does it work? Annu Rev Biochem. 2016 Jun 2;85:685–713. PubMed PMID: 26865532; eng.
  • Zhao YG, Zhang H. ULK1 cycling: the ups and downs of the autophagy response. J Cell Biol. 2016 Dec 19;215(6):757–759. PubMed PMID: 27932574; eng.
  • Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011 Feb;13(2):132–141. PubMed PMID: 21258367; eng.
  • Settembre C, Ballabio A. TFEB regulates autophagy: an integrated coordination of cellular degradation and recycling processes. Autophagy. 2011 Nov;7(11):1379–1381. PubMed PMID: 21785263; eng.
  • Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011 Jun 17;332(6036):1429–1433. PubMed PMID: 21617040; eng.
  • Garcia D, Shaw RJ. AMPK: mechanisms of cellular energy sensing and restoration of metabolic balance. Mol Cell. 2017 Jun 15;66(6):789–800. PubMed PMID: 28622524; eng.
  • Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol. 2018 Feb;19(2):121–135. PubMed PMID: 28974774; eng.
  • Young NP, Kamireddy A, Van Nostrand JL, et al. AMPK governs lineage specification through Tfeb-dependent regulation of lysosomes. Genes Dev. 2016 Mar 01;30(5):535–552. PubMed PMID: 26944679; eng.
  • Fernandez-Mosquera L, Diogo CV, Yambire KF, et al. Acute and chronic mitochondrial respiratory chain deficiency differentially regulate lysosomal biogenesis. Sci Rep. 2017 Mar 27;7:45076. PubMed PMID: 28345620; eng.
  • Hill K, Yuan H, Wang X, et al. Noise-induced loss of hair cells and cochlear synaptopathy are mediated by the activation of AMPK. J Neurosci. 2016 Jul 13;36(28):7497–7510. PubMed PMID: 27413159; eng.
  • McKay SE, Yan W, Nouws J, et al. Auditory pathology in a transgenic mtTFB1 mouse model of mitochondrial deafness. Am J Pathol. 2015 Dec;185(12):3132–3140. PubMed PMID: 26552864; PubMed Central PMCID: PMCPMC5801480. eng.
  • Raimundo N, Song L, Shutt TE, et al. Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell. 2012 Feb 17;148(4):716–726. PubMed PMID: 22341444; PubMed Central PMCID: PMC3285425. eng.
  • Rambold AS, Lippincott-Schwartz J. Mechanisms of mitochondria and autophagy crosstalk. Cell Cycle. 2011 Dec 1;10(23):4032–4038. PubMed PMID: 22101267; eng.
  • Graef M, Nunnari J. Mitochondria regulate autophagy by conserved signalling pathways. Embo J. 2011 Jun 1;30(11):2101–2114. PubMed PMID: 21468027; eng.
  • Graef M, Nunnari J. A role for mitochondria in autophagy regulation. Autophagy. 2011 Oct;7(10):1245–1246. PubMed PMID: 21613823; eng.
  • Te Vruchte D, Speak AO, Wallom KL, et al. Relative acidic compartment volume as a lysosomal storage disorder-associated biomarker. J Clin Invest. 2014 Mar;124(3):1320–1328. PubMed PMID: 24487591; eng.
  • Hurbain I, Romao M, Bergam P, et al. Analyzing lysosome-related organelles by electron microscopy. Methods Mol Biol. 2017;1594:43–71. PubMed PMID: 28456976; eng.
  • Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004 Dec 23;432(7020):1032–1036. PubMed PMID: 15525940; eng.
  • Hesselink RP, Wagenmakers AJ, Drost MR, et al. Lysosomal dysfunction in muscle with special reference to glycogen storage disease type II. Biochim Biophys Acta. 2003 Mar 20;1637(2):164–170. PubMed PMID: 12633905; eng.
  • Cao Q, Yang Y, Zhong XZ, et al. The lysosomal Ca2+ release channel TRPML1 regulates lysosome size by activating calmodulin. J Biol Chem. 2017 May 19;292(20):8424–8435. PubMed PMID: 28360104; eng.
  • Perera RM, Zoncu R. The Lysosome as a regulatory hub. Annu Rev Cell Dev Biol. 2016 Oct 06;32:223–253. PubMed PMID: 27501449; PubMed Central PMCID: PMC5059141. eng.
  • Johnson DE, Ostrowski P, Jaumouille V, et al. The position of lysosomes within the cell determines their luminal pH. J Cell Biol. 2016 Mar 14;212(6):677–692. PubMed PMID: 26975849; eng.
  • Marwaha R, Sharma M. DQ-red BSA trafficking assay in cultured cells to assess cargo delivery to lysosomes. Bio Protoc. 2017 Oct 5;7(19). PubMed PMID: 29082291; eng.
  • Christensen KA, Myers JT, Swanson JA. pH-dependent regulation of lysosomal calcium in macrophages. J Cell Sci. 2002 Feb 1;115(Pt 3):599–607. PubMed PMID: 11861766; eng.
  • Berg TO, Stromhaug E, Lovdal T, et al. Use of glycyl-L-phenylalanine 2-naphthylamide, a lysosome-disrupting cathepsin C substrate, to distinguish between lysosomes and prelysosomal endocytic vacuoles. Biochem J. 1994 May 15;300(Pt 1):229–236. PubMed PMID: 8198538; eng.
  • Medina DL, Di Paola S, Peluso I, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015 Feb 27;17(3):288–299. PubMed PMID: 25720963; Eng.
  • Wang W, Gao Q, Yang M, et al. Up-regulation of lysosomal TRPML1 channels is essential for lysosomal adaptation to nutrient starvation. Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):E1373–81. PubMed PMID: 25733853; eng.
  • Shen D, Wang X, Li X, et al. Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat Commun. 2012 Mar 13;3:731. PubMed PMID: 22415822; eng.
  • Stagi M, Klein ZA, Gould TJ, et al. Lysosome size, motility and stress response regulated by fronto-temporal dementia modifier TMEM106B. Mol Cell Neurosci. 2014 Jul;61:226–240. PubMed PMID: 25066864; eng.
  • Kirkegaard T, Roth AG, Petersen NH, et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature. 2010 Jan 28;463(7280):549–553. PubMed PMID: 20111001; eng.
  • Zdolsek JM, Olsson GM, Brunk UT. Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem Photobiol. 1990 Jan;51(1):67–76. PubMed PMID: 2304980; eng.
  • Zolov SN, Bridges D, Zhang Y, et al. In vivo, PikFYVE generates PI(3,5)P2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17472–17477. PubMed PMID: 23047693; eng.
  • Liu Y, Lai YC, Hill EV, et al. Phosphatidylinositol 3-phosphate 5-kinase (PIKFYVE) is an AMPK target participating in contraction-stimulated glucose uptake in skeletal muscle. Biochem J. 2013 Oct 15;455(2):195–206. PubMed PMID: 23905686; eng.
  • Wingo SN, Gallardo TD, Akbay EA, et al. Somatic LKB1 mutations promote cervical cancer progression. PloS one. 2009;4(4):e5137. PubMed PMID: 19340305; eng.
  • Shaw RJ, Bardeesy N, Manning BD, et al. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell. 2004 Jul;6(1):91–99. PubMed PMID: 15261145.
  • Fogarty S, Hawley SA, Green KA, et al. Calmodulin-dependent protein kinase kinase-beta activates AMPK without forming a stable complex: synergistic effects of Ca2+ and AMP. Biochem J. 2010 Jan 27;426(1):109–118. PubMed PMID: 19958286; eng.
  • Jin N, Lang MJ, Weisman LS. Phosphatidylinositol 3,5-bisphosphate: regulation of cellular events in space and time. Biochem Soc Trans. 2016 Feb;44(1):177–184. PubMed PMID: 26862203; eng.
  • Li X, Wang X, Zhang X, et al. Genetically encoded fluorescent probe to visualize intracellular phosphatidylinositol 3,5-bisphosphate localization and dynamics. Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):21165–21170. PubMed PMID: 24324172; eng.
  • Hammond GR, Takasuga S, Sasaki T, et al. The ML1Nx2 phosphatidylinositol 3,5-bisphosphate probe shows poor selectivity in cells. PloS one. 2015;10(10):e0139957. PubMed PMID: 26460749; PubMed Central PMCID: PMCPMC4604148. eng.
  • Ikonomov OC, Sbrissa D, Delvecchio K, et al. The phosphoinositide kinase PIKfyve is vital in early embryonic development: preimplantation lethality of PIKfyve-/- embryos but normality of PIKfyve± mice. J Biol Chem. 2011 Apr 15;286(15):13404–13413. PubMed PMID: 21349843; eng.
  • Sanders MJ, Ali ZS, Hegarty BD, et al. Defining the mechanism of activation of AMP-activated protein kinase by the small molecule A-769662, a member of the thienopyridone family. J Biol Chem. 2007 Nov 09;282(45):32539–32548. PubMed PMID: 17728241; eng.
  • Goransson O, McBride A, Hawley SA, et al. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem. 2007 Nov 09;282(45):32549–32560. PubMed PMID: 17855357; eng.
  • Kruse SE, Watt WC, Marcinek DJ, et al. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab. 2008 Apr;7(4):312–320. PubMed PMID: 18396137; eng.
  • Yan M, Gingras MC, Dunlop EA, et al. The tumor suppressor folliculin regulates AMPK-dependent metabolic transformation. J Clin Invest. 2014 Jun;124(6):2640–2650. PubMed PMID: 24762438; eng.
  • Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011 Sep 15;25(18):1895–1908. PubMed PMID: 21937710; PubMed Central PMCID: PMC3185962. eng.
  • Gwinn DM, Shackelford DB, Egan DF, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008 Apr 25;30(2):214–226. PubMed PMID: 18439900.
  • Belmokhtar CA, Hillion J, Segal-Bendirdjian E. Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene. 2001 Jun 7;20(26):3354–3362. PubMed PMID: 11423986; eng.
  • McKeague AL, Wilson DJ, Nelson J. Staurosporine-induced apoptosis and hydrogen peroxide-induced necrosis in two human breast cell lines. Br J Cancer. 2003 Jan 13;88(1):125–131. PubMed PMID: 12556971; eng.
  • Zhang X, Cheng X, Yu L, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat Commun. 2016 Jun 30;7:12109. PubMed PMID: 27357649; eng.
  • Grishchuk Y, Pena KA, Coblentz J, et al. Impaired myelination and reduced brain ferric iron in the mouse model of mucolipidosis IV. Dis Model Mech. 2015 Dec;8(12):1591–1601. PubMed PMID: 26398942; eng.
  • Grishchuk Y, Stember KG, Matsunaga A, et al. Retinal dystrophy and optic nerve pathology in the mouse model of mucolipidosis IV. Am J Pathol. 2016 Jan;186(1):199–209. PubMed PMID: 26608452; eng.
  • Garrity AG, Wang W, Collier CM, et al. The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. Elife. 2016 May 23;5. DOI:10.1016/j.tibs.2016.09.001. PubMed PMID: 27213518; PubMed Central PMCID: PMC5123979. eng.
  • Zhang Y, Zolov SN, Chow CY, et al. Loss of Vac14, a regulator of the signaling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17518–17523. PubMed PMID: 17956977; eng.
  • Chow CY, Zhang Y, Dowling JJ, et al. Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature. 2007 Jul 05;448(7149):68–72. PubMed PMID: 17572665; eng.
  • Viscomi C, Bottani E, Civiletto G, et al. In vivo correction of COX deficiency by activation of the AMPK/PGC-1alpha axis. Cell Metab. 2011 Jul 06;14(1):80–90. PubMed PMID: 21723506; eng.
  • Ravi S, Pena KA, Chu CT, et al. Biphasic regulation of lysosomal exocytosis by oxidative stress. Cell Calcium. 2016 Nov;60(5):356–362. PubMed PMID: 27593159; eng.
  • Ge W, Li D, Gao Y, et al. The roles of lysosomes in inflammation and autoimmune diseases. Int Rev Immunol. 2015;34(5):415–431. PubMed PMID: 25075736; eng.
  • Orrenius S, Gogvadze V, Zhivotovsky B. Calcium and mitochondria in the regulation of cell death. Biochem Biophys Res Commun. 2015 Apr 24;460(1):72–81. PubMed PMID: 25998735; eng.
  • Parenti G, Andria G, Ballabio A. Lysosomal storage diseases: from pathophysiology to therapy. Annu Rev Med. 2015;66:471–486. PubMed PMID: 25587658; eng.
  • Venugopal B, Browning MF, Curcio-Morelli C, et al. Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV. Am J Hum Genet. 2007 Nov;81(5):1070–1083. PubMed PMID: 17924347; eng.
  • Diogo CV, Yambire KF, Fernandez Mosquera L, et al. Mitochondrial adventures at the organelle society. Biochem Biophys Res Commun. 2017 Apr 26. DOI:10.1016/j.bbrc.2017.04.124. PubMed PMID: 28456629; eng.
  • Raimundo N, Fernandez-Mosquera L, Yambire KF, et al. Mechanisms of communication between mitochondria and lysosomes. Int J Biochem Cell Biol. 2016 Oct;79:345–349. PubMed PMID: 27613573; eng.
  • Raimundo N, Krisko A. Cross-organelle communication at the core of longevity. Aging (Albany NY). 2018 Jan 22;10(1):15–16. PubMed PMID: 29362289; PubMed Central PMCID: PMCPMC5811256. eng.
  • Peric M, Lovric A, Saric A, et al. TORC1-mediated sensing of chaperone activity alters glucose metabolism and extends lifespan. Aging cell. 2017 Oct;16(5):994–1005. PubMed PMID: 28613034; PubMed Central PMCID: PMCPMC5595670. eng.
  • Peric M, Bou Dib P, Dennerlein S, et al. Crosstalk between cellular compartments protects against proteotoxicity and extends lifespan. Sci Rep. 2016 Jun 27;6:28751. PubMed PMID: 27346163; PubMed Central PMCID: PMCPMC4921836. eng.
  • Wong YC, Ysselstein D, Krainc D. Mitochondria-lysosome contacts regulate mitochondrial fission via RAB7 GTP hydrolysis. Nature. 2018 Feb 15;554(7692):382–386. PubMed PMID: 29364868; eng.
  • Todkar K, Ilamathi HS, Germain M. Mitochondria and lysosomes: discovering bonds. Front Cell Dev Biol. 2017;5:106. PubMed PMID: 29270406; PubMed Central PMCID: PMCPMC5725469. eng.
  • Torres S, Balboa E, Zanlungo S, et al. Lysosomal and mitochondrial liaisons in Niemann-Pick disease. Front Physiol. 2017;8:982. PubMed PMID: 29249985; PubMed Central PMCID: PMCPMC5714892. eng.
  • Soto-Heredero G, Baixauli F, Mittelbrunn M. Interorganelle communication between mitochondria and the endolysosomal system. Front Cell Dev Biol. 2017;5:95. PubMed PMID: 29164114; PubMed Central PMCID: PMCPMC5681906. eng.
  • Murdoch JD, Rostosky CM, Gowrisankaran S, et al. Endophilin-a deficiency induces the Foxo3a-Fbxo32 network in the brain and causes dysregulation of autophagy and the ubiquitin-proteasome system. Cell Rep. 2016 Oct 18;17(4):1071–1086. PubMed PMID: 27720640; PubMed Central PMCID: PMC5366864. eng.
  • Laderoute KR, Amin K, Calaoagan JM, et al. 5ʹ-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol. 2006 Jul;26(14):5336–5347. PubMed PMID: 16809770; eng.
  • Falcon-Perez JM, Nazarian R, Sabatti C, et al. Distribution and dynamics of Lamp1-containing endocytic organelles in fibroblasts deficient in BLOC-3. J Cell Sci. 2005 Nov 15;118(Pt 22):5243–5255. PubMed PMID: 16249233; eng.
  • Lee IH, Cao L, Mostoslavsky R, et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3374–3379. PubMed PMID: 18296641; PubMed Central PMCID: PMCPMC2265142. eng.
  • Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007 Sep-Oct;3(5):452–460. PubMed PMID: 17534139; eng.
  • Raimundo N, Vanharanta S, Aaltonen LA, et al. Downregulation of SRF-FOS-JUNB pathway in fumarate hydratase deficiency and in uterine leiomyomas. Oncogene. 2009 Mar 5;28(9):1261–1273. PubMed PMID: 19151755; eng.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.