Cross-regulation of defective endolysosome trafficking and enhanced autophagy through TFEB in UNC13D deficiency

References

• Klionsky D. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8(11):931–937.
   PubMed Web of Science ®Google Scholar
• Boya P, Gonzalez-Polo RA, Casares N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol. 2005;25(3):1025–1040.
   PubMed Web of Science ®Google Scholar
• Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy. 2011;7(7):673–682.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Cuervo A. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol. 2012;22(8):407–417.
   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
• de Luca A, Smeekens SP, Casagrande A, et al. IL-1 receptor blockade restores autophagy and reduces inflammation in chronic granulomatous disease in mice and in humans. Proc Natl Acad Sci U S A. 2014;111(9):3526–3531.
   PubMed Web of Science ®Google Scholar
• Schneider EM, Lorenz M, Walther P. Autophagy as a hallmark of hemophagocytic disease. In: Gorbunov N, editor. Autophagy: principles, regulation and roles in disease. Hauppauge (NY): Nova Science Publisher; 2012. p. 45–60.
   Google Scholar
• Bode SF, Ammann S, Al-Herz W, et al. The syndrome of hemophagocytic lymphohistiocytosis in primary immunodeficiencies: implications for differential diagnosis and pathogenesis. Haematologica. 2015;100(7):978–988.
   PubMed Web of Science ®Google Scholar
• Lamb CA, Dooley HC, Tooze SA. Endocytosis and autophagy: shared machinery for degradation. Bioessays. 2013;35(1):34–45.
   PubMed Web of Science ®Google Scholar
• Jager S, Bucci C, Tanida I, et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci. 2004;117(Pt 20):4837–4848.
   PubMed Web of Science ®Google 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
• Fader CM, Sanchez D, Furlan M, et al. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic. 2008;9(2):230–250.
   PubMed Web of Science ®Google Scholar
• Szatmari Z, Kis V, Lippai M, et al. Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Mol Biol Cell. 2014;25(4):522–531.
   PubMed Web of Science ®Google Scholar
• Longatti A, Lamb CA, Razi M, et al. TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes. J Cell Biol. 2012;197(5):659–675.
   PubMed Web of Science ®Google Scholar
• Michelet X, Legouis R. Autophagy in endosomal mutants: desperately seeking to survive. Worm. 2012;1(4):216–220.
   PubMedGoogle Scholar
• Itakura E, Mizushima N. Syntaxin 17: the autophagosomal SNARE. Autophagy. 2013;9(6):917–919.
   PubMed Web of Science ®Google Scholar
• Mullock BM, Smith CW, Ihrke G, et al. Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8, and Is required for late endosome-lysosome fusion. Mol Biol Cell. 2000;11(9):3137–3153.
   PubMed Web of Science ®Google Scholar
• Andrews NW. Regulated secretion of conventional lysosomes. Trends Cell Biol. 2000;10(8):316–321.
   PubMed Web of Science ®Google Scholar
• Monteiro P, Rosse C, Castro-Castro A, et al. Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol. 2013;203(6):1063–1079.
   PubMed Web of Science ®Google Scholar
• Settembre C, Fraldi A, Medina D, et al. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol. 2013;14(5):283–296.
   PubMed Web of Science ®Google Scholar
• Sardiello M, Palmieri M, Di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325(5939):473–477.
   PubMed Web of Science ®Google Scholar
• Cuervo A, Mann L, Bonten E, et al. Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor. Embo J. 2003;22(1):47–59.
   PubMed Web of Science ®Google Scholar
• Luzio JP, Hackmann Y, Dieckmann NM, et al. The biogenesis of lysosomes and lysosome-related organelles. Cold Spring Harb Perspect Biol. 2014;6(9):a016840.
   PubMed Web of Science ®Google Scholar
• He C, Klionsky D. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.
   PubMed Web of Science ®Google Scholar
• Bhoopathi P, Chetty C, Gujrati M, et al. Cathepsin B facilitates autophagy-mediated apoptosis in SPARC overexpressed primitive neuroectodermal tumor cells. Cell Death Differ. 2010;17(10):1529–1539.
   PubMed Web of Science ®Google Scholar
• Man SM, Kanneganti TD. Regulation of lysosomal dynamics and autophagy by CTSB/cathepsin B. Autophagy. 2016;12(12):2504–2505.
   PubMed Web of Science ®Google Scholar
• Seglen PO, Gordon PB, Holen I, et al. Hepatocytic autophagy. Biomed Biochim Acta. 1991;50(4–6):373–381.
   PubMedGoogle Scholar
• Sanchez-Wandelmer J, Reggiori F. Amphisomes: out of the autophagosome shadow? Embo J. 2013;32(24):3116–3118.
   PubMed Web of Science ®Google Scholar
• Patel KK, Miyoshi H, Beatty WL, et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. Embo J. 2013;32(24):3130–3144.
   PubMed Web of Science ®Google Scholar
• Cheng XT, Zhou B, Lin MY, et al. Axonal autophagosomes recruit dynein for retrograde transport through fusion with late endosomes. J Cell Biol. 2015;209(3):377–386.
   PubMed Web of Science ®Google Scholar
• Manil-Segalen M, Lefebvre C, Culetto E, et al. Need an ESCRT for autophagosomal maturation? Commun Integr Biol. 2012;5(6):566–571.
   PubMedGoogle 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
• He J, Johnson JL, Monfregola J, et al. Munc13-4 interacts with syntaxin 7 and regulates late endosomal maturation, endosomal signaling, and TLR9-initiated cellular responses. Mol Biol Cell. 2016;27(3):572–587.
   PubMed Web of Science ®Google Scholar
• Neeft M, Wieffer M, de Jong AS, et al. Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. MolBiolCell. 2005;16(2):731–741.
   PubMed Web of Science ®Google Scholar
• Feldmann J, Callebaut I, Raposo G, et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell. 2003;115(4):461–473.
   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
• Koch H, Hofmann K, Brose N. Definition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem J. 2000;349(Pt 1):247–253.
   PubMed Web of Science ®Google Scholar
• Brzezinska AA, Johnson JL, Munafo DB, et al. The Rab27a effectors JFC1/Slp1 and Munc13-4 regulate exocytosis of neutrophil granules. Traffic. 2008;9(12):2151–2164.
   PubMed Web of Science ®Google Scholar
• Johnson JL, Hong H, Monfregola J, et al. MUNC13-4 restricts motility of RAB27A-expressing vesicles to facilitate lipopolysaccharide-induced priming of exocytosis in neutrophils. J Biol Chem. 2010;286:5647–5656.
   PubMed Web of Science ®Google Scholar
• Boswell KL, James DJ, Esquibel JM, et al. Munc13-4 reconstitutes calcium-dependent SNARE-mediated membrane fusion. J Cell Biol. 2012;197(2):301–312.
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Va P, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429–1433.
   PubMed Web of Science ®Google Scholar
• Martina JA, Puertollano R. Rag GTPases mediate amino acid-dependent recruitment of TFEB and MITF to lysosomes. J Cell Biol. 2013;200(4):475–491.
   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
• Spampanato C, Feeney E, Li L, et al. Transcription factor EB (TFEB) is a new therapeutic target for Pompe disease. EMBO Mol Med. 2013;5(5):691–706.
   PubMed Web of Science ®Google Scholar
• Crozat K, Hoebe K, Ugolini S, et al. Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: a mouse model of type 3 familial hemophagocytic lymphohistiocytosis. J Exp Med. 2007;204(4):853–863.
   PubMed Web of Science ®Google Scholar
• Mudrakola HV, Zhang K, Cui B. Optically resolving individual microtubules in live axons. Structure. 2009;17(11):1433–1441.
   PubMed Web of Science ®Google Scholar
• Lencer WI, Weyer P, Verkman AS, et al. FITC-dextran as a probe for endosome function and localization in kidney. Am J Physiol. 1990;258(2 Pt 1):C309–C317.
   PubMedGoogle Scholar
• Nakamura N, Lill JR, Phung Q, et al. Endosomes are specialized platforms for bacterial sensing and NOD2 signalling. Nature. 2014;509(7499):240–244.
   PubMed Web of Science ®Google Scholar
• Jaiswal JK, Andrews NW, Simon SM. Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J Cell Biol. 2002;159(4):625–635.
   PubMed Web of Science ®Google Scholar
• Pillay CS, Elliott E, Dennison C. Endolysosomal proteolysis and its regulation. Biochem J. 2002;363(Pt 3):417–429.
   PubMed Web of Science ®Google Scholar
• Johnson DE, Ostrowski P, Jaumouille V, et al. The position of lysosomes within the cell determines their luminal pH. J Cell Biol. 2016;212(6):677–692.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222.
   PubMed Web of Science ®Google Scholar
• Bjorkoy G, Lamark T, Pankiv S, et al. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol. 2009;452:181–197.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213–223.
   PubMed Web of Science ®Google Scholar
• Garrett JP, Fung I, Rupon J, et al. Presentation of hemophagocytic lymphohistiocytosis due to a novel MUNC 13-4 mutation masked by partial therapeutic immunosuppression. Pediatr Rheumatol Online J. 2012;10(1):13.
   PubMedGoogle Scholar
• Sandri M. Autophagy in skeletal muscle. FEBS Lett. 2010;584(7):1411–1416.
   PubMed Web of Science ®Google Scholar
• Longatti A, Tooze SA. Recycling endosomes contribute to autophagosome formation. Autophagy. 2012;8(11):1682–1683.
   PubMed Web of Science ®Google Scholar
• Diao J, Liu R, Rong Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015;520(7548):563–566.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Ahmed Z, Bradfute SB, et al. Pharmaceutical screen identifies novel target processes for activation of autophagy with a broad translational potential. Nat Commun. 2015;6:8620.
   PubMed Web of Science ®Google Scholar
• Fan Y, Lu H, Liang W, et al. Endothelial TFEB (transcription factor EB) positively regulates postischemic angiogenesis. Circ Res. 2018;122(7):945–957.
   PubMed Web of Science ®Google Scholar
• Martina JA, Diab HI, Lishu L, et al. The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris. Sci Signal. 2014;7(309):ra9.
   PubMed Web of Science ®Google Scholar
• Sha Y, Rao L, Settembre C, et al. STUB1 regulates TFEB-induced autophagy-lysosome pathway. Embo J. 2017;36(17):2544–2552.
   PubMed Web of Science ®Google Scholar
• Wada S, Neinast M, Jang C, et al. The tumor suppressor FLCN mediates an alternate mTOR pathway to regulate browning of adipose tissue. Genes Dev. 2016;30(22):2551–2564.
   PubMed Web of Science ®Google Scholar
• Bartolomeo R, Cinque L, De Leonibus C, et al. mTORC1 hyperactivation arrests bone growth in lysosomal storage disorders by suppressing autophagy. J Clin Invest. 2017;127(10):3717–3729.
   PubMed Web of Science ®Google Scholar
• Palmieri M, Pal R, Nelvagal HR, et al. mTORC1-independent TFEB activation via Akt inhibition promotes cellular clearance in neurodegenerative storage diseases. Nat Commun. 2017;8:14338.
   PubMed Web of Science ®Google Scholar
• Liu P, Liu K, Gu H, et al. High autophagic flux guards ESC identity through coordinating autophagy machinery gene program by FOXO1. Cell Death Differ. 2017;24(10):1672–1680.
   PubMed Web of Science ®Google Scholar
• Kalatzis V, Cherqui S, Antignac C, et al. 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
• Kalatzis V, Nevo N, Cherqui S, et al. Molecular pathogenesis of cystinosis: effect of CTNS mutations on the transport activity and subcellular localization of cystinosin. Hum Mol Genet. 2004;13(13):1361–1371.
   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
• Higashio H, Nishimura N, Ishizaki H, et al. Doc2 alpha and Munc13-4 regulate Ca(2+) -dependent secretory lysosome exocytosis in mast cells. J Immunol. 2008;180(7):4774–4784.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 2012;151(6):1256–1269.
   PubMed Web of Science ®Google Scholar
• Furuta N, Fujita N, Noda T, et al. Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Mol Biol Cell. 2010;21(6):1001–1010.
   PubMed Web of Science ®Google Scholar
• Jain A, Lamark T, Sjottem E, et al. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem. 2010;285(29):22576–22591.
   PubMed Web of Science ®Google Scholar
• Weaver LK, Behrens EM. Hyperinflammation, rather than hemophagocytosis, is the common link between macrophage activation syndrome and hemophagocytic lymphohistiocytosis. Curr Opin Rheumatol. 2014;26(5):562–569.
   PubMed Web of Science ®Google Scholar
• Zhang K, Biroschak J, Glass DN, et al. Macrophage activation syndrome in patients with systemic juvenile idiopathic arthritis is associated with MUNC13-4 polymorphisms. Arthritis Rheum. 2008;58(9):2892–2896.
   PubMed Web of Science ®Google Scholar
• Schneider EM, Flacke S, Liu F, et al. Autophagy and ATP-induced anti-apoptosis in antigen presenting cells (APC) follows the cytokine storm in patients after major trauma. J Cell Commun Signal. 2011;5(2):145–156.
   PubMed Web of Science ®Google Scholar
• Wei H, Kim SJ, Zhang Z, et al. ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum Mol Genet. 2008;17(4):469–477.
   PubMed Web of Science ®Google Scholar
• Settembre C, Fraldi A, Jahreiss L, et al. A block of autophagy in lysosomal storage disorders. Hum Mol Genet. 2008;17(1):119–129.
   PubMed Web of Science ®Google Scholar
• Venugopal B, Mesires NT, Kennedy JC, et al. Chaperone-mediated autophagy is defective in mucolipidosis type IV. J Cell Physiol. 2009;219(2):344–353.
   PubMed Web of Science ®Google Scholar
• Medina DL, Fraldi A, Bouche V, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell. 2011;21(3):421–430.
   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. Nephrol Dial Transplant. 2010;25(4):1059–1066.
   PubMed Web of Science ®Google Scholar
• Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, et al. Regulation of TFEB and V-ATPases by mTORC1. Embo J. 2011;30(16):3242–3258.
   PubMed Web of Science ®Google Scholar