DYNC1LI2 regulates localization of the chaperone-mediated autophagy receptor LAMP2A and improves cellular homeostasis in cystinosis

References

• Town M, Jean G, Cherqui S, et al. A novel gene encoding an integral membrane protein is mutated in nephropathic cystinosis. Nat Genet. 1998;18(4):319–324.
   PubMed Web of Science ®Google Scholar
• Kalatzis V. Cystinosin, the protein defective in cystinosis, is a H+-driven lysosomal cystine transporter. EMBO J. 2001;20(21):5940–5949.
   PubMed Web of Science ®Google Scholar
• Napolitano G, Johnson JL, He J, et al. Impairment of chaperone-mediated autophagy leads to selective lysosomal degradation defects in the lysosomal storage disease cystinosis. EMBO Mol Med. 2015;7(2):158–174.
   PubMed Web of Science ®Google Scholar
• Andrzejewska Z, Nevo N, Thomas L, et al. Cystinosin is a component of the vacuolar H+-ATPase-ragulator-rag complex controlling mammalian target of rapamycin complex 1 signaling. J Am Soc Nephrol. 2016;27(6):1678–1688.
   PubMed Web of Science ®Google Scholar
• Rega LR, Polishchuk E, Montefusco S, et al. Activation of the transcription factor EB rescues lysosomal abnormalities in cystinotic kidney cells. Kidney Int. 2016;89(4):862–873.
   PubMed Web of Science ®Google Scholar
• Gahl WA, Thoene JG, Schneider JA. Cystinosis. N Engl J Med. 2002;347(2):111–121.
   PubMed Web of Science ®Google Scholar
• Da Silva V, Zurbrügg R, Lavanchy P, et al. Long-term treatment of infantile nephropathic cystinosis with cysteamine. N Engl J Med. 1985;313(23):1460–1463.
   PubMed Web of Science ®Google Scholar
• Cherqui S, Courtoy PJ. The renal Fanconi syndrome in cystinosis: pathogenic insights and therapeutic perspectives. Nat Rev Nephrol. 2017;13(2):115–131.
   PubMed Web of Science ®Google Scholar
• Cherqui S. Cysteamine therapy: a treatment for cystinosis, not a cure. Kidney Int. 2012;81(2):127–129.
   PubMed Web of Science ®Google Scholar
• Vaisbich M, Pache de Faria Guimaraes L, Shimizu M, et al. Oxidative stress in cystinosis patients. Nephron Extra. 2011;1(1):73–77.
   PubMedGoogle Scholar
• Zhang J, Johnson JL, He J, et al. Cystinosin, the small GTPase Rab11, and the Rab7 effector RILP regulate intracellular trafficking of the chaperone-mediated autophagy receptor LAMP2A. J Biol Chem. 2017;292(25):10328–10346.
   PubMed Web of Science ®Google Scholar
• Johnson J, Napolitano G, Monfregola J, et al. Upregulation of the Rab27a-dependent trafficking and secretory mechanisms improves lysosomal transport, alleviates endoplasmic reticulum stress, and reduces lysosome overload in cystinosis. Mol Cell Biol. 2013;33(15):2950–2962.
   PubMed Web of Science ®Google Scholar
• Hook P, Vallee RB. The dynein family at a glance. J Cell Sci. 2006;119(21):4369–4371.
   PubMed Web of Science ®Google Scholar
• Holzbaur EL, Hammarback JA, Paschal BM, et al. Correction: homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature. 1992;360(6405):695.
   PubMed Web of Science ®Google Scholar
• Holzbaur EL, Vallee RB. DYNEINS: molecular structure and cellular function. Annu Rev Cell Biol. 1994;10:339–372.
   PubMedGoogle Scholar
• King SJ, Bonilla M, Rodgers ME, et al. Subunit organization in cytoplasmic dynein subcomplexes. Protein Sci. 2002;11(5):1239–1250.
   PubMed Web of Science ®Google Scholar
• Wang Y, Huynh W, Skokan TD, et al. CRACR2a is a calcium-activated dynein adaptor protein that regulates endocytic traffic. J Cell Biol. 2019;218(5):1619–1633.
   PubMed Web of Science ®Google Scholar
• Olenick MA, Holzbaur ELF. Dynein activators and adaptors at a glance. J Cell Sci. 2019;132(6):6.
   Web of Science ®Google Scholar
• Olenick MA, Tokito M, Boczkowska M, et al. Hook adaptors induce unidirectional processive motility by enhancing the dynein-dynactin interaction. J Biol Chem. 2016;291(35):18239–18251.
   PubMed Web of Science ®Google Scholar
• McKenney RJ, Huynh W, Tanenbaum ME, et al. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science. 2014;345(6194):337–341.
   PubMed Web of Science ®Google Scholar
• Mische S, He Y, Ma L, et al. Dynein light intermediate chain: an essential subunit that contributes to spindle checkpoint inactivation. Mol Biol Cell. 2008;19(11):4918–4929.
   PubMed Web of Science ®Google Scholar
• Perrone CA, Tritschler D, Taulman P, et al. A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in chlamydomonas and mammalian cells. Mol Biol Cell. 2003;14(5):2041–2056.
   PubMed Web of Science ®Google Scholar
• Purohit A, Tynan SH, Vallee R, et al. Direct interaction of pericentrin with cytoplasmic dynein light intermediate chain contributes to mitotic spindle organization. J Cell Biol. 1999;147(3):481–492.
   PubMed Web of Science ®Google Scholar
• Bielli A, Thornqvist P-O, Hendrick AG, et al. The small GTPase Rab4A interacts with the central region of cytoplasmic dynein light intermediate chain-1. Biochem Biophys Res Commun. 2001;281(5):1141–1153.
   PubMed Web of Science ®Google Scholar
• Goncalves JC, Dantas TJ, Vallee RB. Distinct roles for dynein light intermediate chains in neurogenesis, migration, and terminal somal translocation. J Cell Biol. 2019;218(3):808–819.
   PubMed Web of Science ®Google Scholar
• Grissom PM, Vaisberg EA, McIntosh JR. Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2. Mol Biol Cell. 2002;13(3):817–829.
   PubMed Web of Science ®Google Scholar
• Jones LA, Villemant C, Starborg T, et al. Dynein light intermediate chains maintain spindle bipolarity by functioning in centriole cohesion. J Cell Biol. 2014;207(4):499–516.
   PubMed Web of Science ®Google Scholar
• Palmer KJ, Hughes H, Stephens DJ. Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol Biol Cell. 2009;20(12):2885–2899.
   PubMed Web of Science ®Google Scholar
• Schroeder CM, Ostrem JM, Hertz NT, et al. A Ras-like domain in the light intermediate chain bridges the dynein motor to a cargo-binding region. Elife. 2014;3:e03351.
   PubMed Web of Science ®Google Scholar
• Tan SC, Scherer J, Vallee RB. Recruitment of dynein to late endosomes and lysosomes through light intermediate chains. Mol Biol Cell. 2011;22(4):467–477.
   PubMed Web of Science ®Google Scholar
• Horgan CP, Hanscom SR, Jolly RS, et al. Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J Cell Sci. 2010;123(2):181–191.
   PubMed Web of Science ®Google Scholar
• Horgan CP, Hanscom SR, Jolly RS, et al. Rab11-FIP3 binds dynein light intermediate chain 2 and its overexpression fragments the Golgi complex. Biochem Biophys Res Commun. 2010;394(2):387–392.
   PubMed Web of Science ®Google Scholar
• Lee I-G, Olenick MA, Boczkowska M, et al. A conserved interaction of the dynein light intermediate chain with dynein-dynactin effectors necessary for processivity. Nat Commun. 2018;9(1):986.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Cuervo AM. The coming of age of chaperone-mediated autophagy. Nat Rev Mol Cell Biol. 2018;19(6):365–381.
   PubMed Web of Science ®Google Scholar
• Kirchner P, Bourdenx M, Madrigal-Matute J, et al. Proteome-wide analysis of chaperone-mediated autophagy targeting motifs. PLoS Biol. 2019;17(5):e3000301.
   PubMed Web of Science ®Google Scholar
• Cuervo A, Dice J. Regulation of lamp2a levels in the lysosomal membrane. Traffic. 2000;1(7):570–583.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Bandyopadhyay U, Sridhar S, et al. Chaperone-mediated autophagy at a glance. J Cell Sci. 2011;124(4):495–499.
   PubMed Web of Science ®Google Scholar
• Kiffin R, Christian C, Knecht E, et al. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell. 2004;15(11):4829–4840.
   PubMed Web of Science ®Google Scholar
• Zhang J, He J, Johnson JL, et al. Chaperone-mediated autophagy upregulation rescues megalin expression and localization in cystinotic proximal tubule cells. Front Endocrinol (Lausanne). 2019;10:21.
   PubMed Web of Science ®Google Scholar
• Scherer J, Yi J, Vallee RB. PKA-dependent dynein switching from lysosomes to adenovirus: a novel form of host–virus competition. J Cell Biol. 2014;205(2):163–177.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Cuervo A. Chaperone-mediated autophagy. Methods Mol Biol. 2008;445:227–244.
   PubMedGoogle Scholar
• Malkus K, Ischiropoulos H. Regional deficiencies in chaperone-mediated autophagy underlie α-synuclein aggregation and neurodegeneration. Neurobiol Dis. 2012;46(3):732–744.
   PubMed Web of Science ®Google Scholar
• Yan W, Frank CL, Korth MJ, et al. Control of PERK eIF2 kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci USA. 2002;99(25):15920–15925.
   PubMed Web of Science ®Google Scholar
• Fusakio ME, Willy JA, Wang Y, et al. Transcription factor ATF4 directs basal and stress-induced gene expression in the unfolded protein response and cholesterol metabolism in the liver. Mol Biol Cell. 2016;27(9):1536–1551.
   PubMed Web of Science ®Google Scholar
• Harding HP, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. 2003;11(3):619–633.
   PubMed Web of Science ®Google Scholar
• Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12(1):9–14.
   PubMed Web of Science ®Google Scholar
• Bellomo F, Signorile A, Tamma G, et al. Impact of atypical mitochondrial cyclic-AMP level in nephropathic cystinosis. Cell Mol Life Sci. 2018;75(18):3411–3422.
   PubMed Web of Science ®Google Scholar
• Heeman B, Van den Haute C, Aelvoet S-A, et al. Depletion of PINK1 affects mitochondrial metabolism, calcium homeostasis and energy maintenance. J Cell Sci. 2011;124(7):1115–1125.
   PubMed Web of Science ®Google Scholar
• Suen D-F, Norris KL, Youle RJ. Mitochondrial dynamics and apoptosis. Genes Dev. 2008;22(12):1577–1590.
   PubMed Web of Science ®Google Scholar
• Gaide Chevronnay HP, Janssens V, Van Der Smissen P, et al. Time course of pathogenic and adaptation mechanisms in cystinotic mouse kidneys. J Am Soc Nephrol. 2014;25(6):1256–1269.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Cuervo A. Methods to monitor chaperone-mediated autophagy. Methods Enzymol. 2009;452:297–324.
   PubMed Web of Science ®Google Scholar
• Johansson M, Rocha N, Zwart W, et al. Activation of endosomal dynein motors by stepwise assembly of Rab7–RILP–p150Glued, ORP1L, and the receptor βlll spectrin. J Cell Biol. 2007;176(4):459–471.
   PubMed Web of Science ®Google Scholar
• Nevo N, Chol M, Bailleux A, et al. Renal phenotype of the cystinosis mouse model is dependent upon genetic background. NephrolDialTransplant. 2010;25(4):1059–1066.
   Google Scholar
• Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249–264.
   PubMed Web of Science ®Google Scholar
• Johnson JL, He J, Ramadass M, et al. Munc13-4 is a Rab11-binding protein that regulates Rab11-positive vesicle trafficking and docking at the plasma membrane. J Biol Chem. 2016;291(7):3423–3438.
   PubMed Web of Science ®Google Scholar