Endolysosomes Are the Principal Intracellular Sites of Acid Hydrolase Activity

Current Biology

Volumn 26, Issue 17, 2016, Pages 2233-2245

  Bright, Nicholas A ^a   Davis, Luther J ^a   Luzio, J Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASE;

ENDOSOME; FIBROBLAST; HELA CELL LINE; HUMAN; LYSOSOME; MCF-7 CELL LINE; METABOLISM;

ENDOSOMES; FIBROBLASTS; HELA CELLS; HUMANS; HYDROLASES; LYSOSOMES; MCF-7 CELLS;

EID: 84995920421     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.06.046     Document Type: Article

References (50)

1. 1 de Duve, C., The lysosome turns fifty. Nat. Cell Biol. 7 (2005), 847–849.
2. 2 Sardiello, M., Palmieri, M., di Ronza, A., Medina, D.L., Valenza, M., Gennarino, V.A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R.S., et al. A gene network regulating lysosomal biogenesis and function. Science 325 (2009), 473–477.
3. 3 Settembre, C., Fraldi, A., Medina, D.L., Ballabio, A., Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14 (2013), 283–296.
4. 4 Settembre, C., Zoncu, R., Medina, D.L., Vetrini, F., Erdin, S., Erdin, S., Huynh, T., Ferron, M., Karsenty, G., Vellard, M.C., et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31 (2012), 1095–1108.
5. 5 Roczniak-Ferguson, A., Petit, C.S., Froehlich, F., Qian, S., Ky, J., Angarola, B., Walther, T.C., Ferguson, S.M., The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal., 5, 2012, ra42.
6. 6 Bright, N.A., Gratian, M.J., Luzio, J.P., Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells. Curr. Biol. 15 (2005), 360–365.
7. 7 Luzio, J.P., Pryor, P.R., Bright, N.A., Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8 (2007), 622–632.
8. 8 Huotari, J., Helenius, A., Endosome maturation. EMBO J. 30 (2011), 3481–3500.
9. 9 Bright, N.A., Reaves, B.J., Mullock, B.M., Luzio, J.P., Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles. J. Cell Sci. 110 (1997), 2027–2040.
10. 10 Creasy, B.M., Hartmann, C.B., White, F.K., McCoy, K.L., New assay using fluorogenic substrates and immunofluorescence staining to measure cysteine cathepsin activity in live cell subpopulations. Cytometry A 71 (2007), 114–123.
11. 11 Pols, M.S., ten Brink, C., Gosavi, P., Oorschot, V., Klumperman, J., The HOPS proteins hVps41 and hVps39 are required for homotypic and heterotypic late endosome fusion. Traffic 14 (2013), 219–232.
12. 12 Jadot, M., Colmant, C., Wattiaux-De Coninck, S., Wattiaux, R., Intralysosomal hydrolysis of glycyl-L-phenylalanine 2-naphthylamide. Biochem. J. 219 (1984), 965–970.
13. 13 Haller, T., Dietl, P., Deetjen, P., Völkl, H., The lysosomal compartment as intracellular calcium store in MDCK cells: a possible involvement in InsP3-mediated Ca2+ release. Cell Calcium 19 (1996), 157–165.
14. 14 Steinberg, B.E., Huynh, K.K., Brodovitch, A., Jabs, S., Stauber, T., Jentsch, T.J., Grinstein, S., A cation counterflux supports lysosomal acidification. J. Cell Biol. 189 (2010), 1171–1186.
15. 15 López-Sanjurjo, C.I., Tovey, S.C., Prole, D.L., Taylor, C.W., Lysosomes shape Ins(1,4,5)P3-evoked Ca2+ signals by selectively sequestering Ca2+ released from the endoplasmic reticulum. J. Cell Sci. 126 (2013), 289–300.
16. 16 Penny, C.J., Kilpatrick, B.S., Han, J.M., Sneyd, J., Patel, S., A computational model of lysosome-ER Ca2+ microdomains. J. Cell Sci. 127 (2014), 2934–2943.
17. 17 Vázquez, C.L., Colombo, M.I., Assays to assess autophagy induction and fusion of autophagic vacuoles with a degradative compartment, using monodansylcadaverine (MDC) and DQ-BSA. Methods Enzymol. 452 (2009), 85–95.
18. 18 Griffiths, G., Hoflack, B., Simons, K., Mellman, I., Kornfeld, S., The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52 (1988), 329–341.
19. 19 Griffiths, G., Matteoni, R., Back, R., Hoflack, B., Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell Sci. 95 (1990), 441–461.
20. 20 Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., Gruenberg, J., A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392 (1998), 193–197.
21. 21 Ohkuma, S., Poole, B., Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J. Cell Biol. 90 (1981), 656–664.
22. 22 Anderson, R.G., Falck, J.R., Goldstein, J.L., Brown, M.S., Visualization of acidic organelles in intact cells by electron microscopy. Proc. Natl. Acad. Sci. USA 81 (1984), 4838–4842.
23. 23 Higuchi, T., Nishikawa, J., Inoue, H., Sucrose induces vesicle accumulation and autophagy. J. Cell. Biochem. 116 (2015), 609–617.
24. 24 Gan, Z., Ram, S., Vaccaro, C., Ober, R.J., Ward, E.S., Analyses of the recycling receptor, FcRn, in live cells reveal novel pathways for lysosomal delivery. Traffic 10 (2009), 600–614.
25. 25 Kaufmann, A.M., Krise, J.P., Niemann-Pick C1 functions in regulating lysosomal amine content. J. Biol. Chem. 283 (2008), 24584–24593.
26. 26 Berg, T., Gjøen, T., Bakke, O., Physiological functions of endosomal proteolysis. Biochem. J. 307 (1995), 313–326.
27. 27 Humphries, W.H. 4th, Szymanski, C.J., Payne, C.K., Endo-lysosomal vesicles positive for Rab7 and LAMP1 are terminal vesicles for the transport of dextran. PLoS ONE, 6, 2011, e26626.
28. 28 Casciola-Rosen, L.A., Renfrew, C.A., Hubbard, A.L., Lumenal labeling of rat hepatocyte endocytic compartments. Distribution of several acid hydrolases and membrane receptors. J. Biol. Chem. 267 (1992), 11856–11864.
29. 29 Galmes, R., ten Brink, C., Oorschot, V., Veenendaal, T., Jonker, C., van der Sluijs, P., Klumperman, J., Vps33B is required for delivery of endocytosed cargo to lysosomes. Traffic 16 (2015), 1288–1305.
30. 30 Hellevik, T., Martinez, I., Olsen, R., Toh, B.H., Webster, P., Smedsrød, B., Transport of residual endocytosed products into terminal lysosomes occurs slowly in rat liver endothelial cells. Hepatology 28 (1998), 1378–1389.
31. 31 Griffiths, G., On vesicles and membrane compartments. Protoplasma 195 (1996), 37–58.
32. 32 Tjelle, T.E., Brech, A., Juvet, L.K., Griffiths, G., Berg, T., Isolation and characterization of early endosomes, late endosomes and terminal lysosomes: their role in protein degradation. J. Cell Sci. 109 (1996), 2905–2914.
33. 33 Butor, C., Griffiths, G., Aronson, N.N. Jr., Varki, A., Co-localization of hydrolytic enzymes with widely disparate pH optima: implications for the regulation of lysosomal pH. J. Cell Sci. 108 (1995), 2213–2219.
34. 34 Hirota, Y., Masuyama, N., Kuronita, T., Fujita, H., Himeno, M., Tanaka, Y., Analysis of post-lysosomal compartments. Biochem. Biophys. Res. Commun. 314 (2004), 306–312.
35. 35 Johnson, D.E., Ostrowski, P., Jaumouillé, V., Grinstein, S., The position of lysosomes within the cell determines their luminal pH. J. Cell Biol. 212 (2016), 677–692.
36. 36 Pryor, P.R., Mullock, B.M., Bright, N.A., Gray, S.R., Luzio, J.P., The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149 (2000), 1053–1062.
37. 37 Carnell, M., Zech, T., Calaminus, S.D., Ura, S., Hagedorn, M., Johnston, S.A., May, R.C., Soldati, T., Machesky, L.M., Insall, R.H., Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis. J. Cell Biol. 193 (2011), 831–839.
38. 38 Stransky, L.A., Forgac, M., Amino Acid Availability Modulates Vacuolar H+-ATPase Assembly. J. Biol. Chem. 290 (2015), 27360–27369.
39. 39 De Luca, M., Cogli, L., Progida, C., Nisi, V., Pascolutti, R., Sigismund, S., Di Fiore, P.P., Bucci, C., RILP regulates vacuolar ATPase through interaction with the V1G1 subunit. J. Cell Sci. 127 (2014), 2697–2708.
40. 40 Miller, A., Schafer, J., Upchurch, C., Spooner, E., Huynh, J., Hernandez, S., McLaughlin, B., Oden, L., Fares, H., Mucolipidosis type IV protein TRPML1-dependent lysosome formation. Traffic 16 (2015), 284–297.
41. 41 Mousavi, S.A., Brech, A., Berg, T., Kjeken, R., Phosphoinositide 3-kinase regulates maturation of lysosomes in rat hepatocytes. Biochem. J. 372 (2003), 861–869.
42. 42 Jahreiss, L., Menzies, F.M., Rubinsztein, D.C., The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9 (2008), 574–587.
43. 43 Yu, L., McPhee, C.K., Zheng, L., Mardones, G.A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F., et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465 (2010), 942–946.
44. 44 Rong, Y., Liu, M., Ma, L., Du, W., Zhang, H., Tian, Y., Cao, Z., Li, Y., Ren, H., Zhang, C., et al. Clathrin and phosphatidylinositol-4,5-bisphosphate regulate autophagic lysosome reformation. Nat. Cell Biol. 14 (2012), 924–934.
45. 45 Chen, Y., Yu, L., Autophagic lysosome reformation. Exp. Cell Res. 319 (2013), 142–146.
46. 46 Chang, J., Lee, S., Blackstone, C., Spastic paraplegia proteins spastizin and spatacsin mediate autophagic lysosome reformation. J. Clin. Invest. 124 (2014), 5249–5262.
47. 47 Schulze, R.J., Weller, S.G., Schroeder, B., Krueger, E.W., Chi, S., Casey, C.A., McNiven, M.A., Lipid droplet breakdown requires dynamin 2 for vesiculation of autolysosomal tubules in hepatocytes. J. Cell Biol. 203 (2013), 315–326.
48. 48 Bandyopadhyay, D., Cyphersmith, A., Zapata, J.A., Kim, Y.J., Payne, C.K., Lysosome transport as a function of lysosome diameter. PLoS ONE, 9, 2014, e86847.
49. 49 Cohn, Z.A., Ehrenreich, B.A., The uptake, storage, and intracellular hydrolysis of carbohydrates by macrophages. J. Exp. Med. 129 (1969), 201–225.
50. 50 Montgomery, R.R., Webster, P., Mellman, I., Accumulation of indigestible substances reduces fusion competence of macrophage lysosomes. J. Immunol. 147 (1991), 3087–3095.