Cathepsin D and its newly identified transport receptor SEZ6L2 can modulate neurite outgrowth

Journal of Cell Science

Volumn 129, Issue 3, 2016, Pages 557-568

  Boonen, Marielle ^a   Staudt, Catherine ^a   Gilis, Florentine ^a   Oorschot, Viola ^b   Klumperman, Judith ^b   Jadot, Michel ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Lysosomal hydrolase; Mannose 6 phosphate independent; Transport receptor

Indexed keywords

CATHEPSIN D; LYSOSOME ENZYME; MEMBRANE PROTEIN; PROTEIN SEZ6L2; SOMATOMEDIN B RECEPTOR; TYROSINE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 1 PHOSPHOTRANSFERASE; ALPHA-BETA GLCNAC-1-PHOSPHOTRANSFERASE, HUMAN; CARRIER PROTEIN; PHOSPHOTRANSFERASE; SEZ6L2 PROTEIN, HUMAN; URIDINE DIPHOSPHATE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; COATED VESICLE; CONTROLLED STUDY; ENDOSOME; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; INTERNALIZATION; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROBLASTOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; CELL LINE; LYSOSOME; METABOLISM; NEURITE; NEUROBLASTOMA; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; BRAIN; CARRIER PROTEINS; CATHEPSIN D; CELL LINE; CELL LINE, TUMOR; ENDOSOMES; HELA CELLS; HUMANS; LYSOSOMES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NEURITES; NEUROBLASTOMA; PROTEIN TRANSPORT; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS); URIDINE DIPHOSPHATE;

EID: 84957627541     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.179374     Document Type: Article

References (52)

1. Authier, F., Mort, J. S., Bell, A. W., Posner, B. I. and Bergeron, J. J. (1995). Proteolysis of glucagon within hepatic endosomes by membrane-associated cathepsins B and D. J. Biol. Chem. 270, 15798-15807.
2. Baranski, T. J., Faust, P. L. and Kornfeld, S. (1990). Generation of a lysosomal enzyme targeting signal in the secretory protein pepsinogen. Cell 63, 281-291.
3. Beaujouin, M., Prébois, C., Derocq, D., Laurent-Matha, V., Masson, O., Pattingre, S., Coopman, P., Bettache, N., Grossfield, J., Hollingsworth, R. E. et al. (2010). Pro-cathepsin D interacts with the extracellular domain of the beta chain of LRP1 and promotes LRP1-dependent fibroblast outgrowth. J. Cell Sci. 123, 3336-3346.
4. Blitz, A. L., Fine, R. E. and Toselli, P. A. (1977). Evidence that coated vesicles isolated from brain are calcium-sequestering organelles resembling sarcoplasmic reticulum. J. Cell Biol. 75, 135-147.
5. Boonen, M., Rezende de Castro, R., Cuvelier, G., Hamer, I. and Jadot, M. (2008). A dileucine signal situated in the C-terminal tail of the lysosomal membrane protein p40 is responsible for its targeting to lysosomes. Biochem. J. 414, 431-440.
6. Boonen, M., Vogel, P., Platt, K. A., Dahms, N. and Kornfeld, S. (2009). Mice lacking mannose 6-phosphate uncovering enzyme activity have a milder phenotype than mice deficient for N-acetylglucosamine-1-phosphotransferase activity. Mol. Biol. Cell. 20, 4381-4389.
7. Boonen, M., van Meel, E., Oorschot, V., Klumperman, J. and Kornfeld, S. (2011). Vacuolization of mucolipidosis type II mouse exocrine gland cells represents accumulation of autolysosomes. Mol. Biol. Cell 22, 1135-1147.
8. Braulke, T. and Bonifacino, J. S. (2009). Sorting of lysosomal proteins. Biochim. Biophys. Acta 1793, 605-614.
9. Canuel, M., Korkidakis, A., Konnyu, K. and Morales, C. R. (2008). Sortilin mediates the lysosomal targeting of cathepsins D and H. Biochem. Biophys. Res. Commun. 373, 292-297.
10. Cullen, V., Lindfors, M., Ng, J., Paetau, A., Swinton, E., Kolodzeij, P., Boston, H., Saftig, P., Woulfe, J., Feany, M. B. et al. (2009). Cathepsin D expression level affects alpha-synuclein processing, aggregation, and toxicity in vivo. Mol. Brain. 2, 5.
11. Derocq, D., Prébois, C., Beaujouin, M., Laurent-Matha, V., Pattingre, S., Smith, G. K. and Liaudet-Coopman, E. (2012). Cathepsin D is partly endocytosed by the LRP1 receptor and inhibits LRP1-regulated intramembrane proteolysis. Oncogene 31, 3202-3212.
12. Diment, S. and Stahl, P. (1985). Macrophage endosomes contain proteases which degrade endocytosed protein ligands. J. Biol. Chem. 260, 15311-15317.
13. Dittmer, F., Ulbrich, E. J., Hafner, A., Schmahl, W., Meister, T., Pohlmann, R. and von Figura, K. (1999). Alternative mechanisms for trafficking of lysosomal enzymes in mannose 6-phosphate receptor-deficient mice are cell type-specific. J. Cell Sci. 112, 1591-1597.
14. Ghosh, P., Dahms, N. M. and Kornfeld, S. (2003). Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4, 202-213.
15. Glickman, J. N. and Kornfeld, S. (1993). Mannose 6-phosphate-independent targeting of lysosomal enzymes in I-cell disease B lymphoblasts. J. Cell Biol. 123, 99-108.
16. Gunnersen, J. M., Kim, M. H., Fuller, S. J., De Silva, M., Britto, J. M., Hammond, V. E., Davies, P. J., Petrou, S., Faber, E. S. L., Sah, P. et al. (2007). Sez-6 proteins affect dendritic arborization patterns and excitability of cortical pyramidal neurons. Neuron 56, 621-639.
17. Hamer, I. and Jadot, M. (2005). Endolysosomal transport of newly-synthesized cathepsin D in a sucrose model of lysosomal storage. Exp. Cell Res. 309, 284-295.
18. Koch, S., Molchanova, S. M., Wright, A. K., Edwards, A., Cooper, J. D., Taira, T., Gillingwater, T. H. and Tyynelä, J. (2011). Morphologic and functional correlates of synaptic pathology in the cathepsin D knockout mouse model of congenital neuronal ceroid lipofuscinosis. J. Neuropathol. Exp. Neurol. 70, 1089-1096.
19. Koch, S., Scifo, E., Rokka, A., Trippner, P., Lindfors, M., Korhonen, R., Corthals, G. L., Virtanen, I., Lalowski, M. and Tyynelä, J. (2013). Cathepsin D deficiency induces cytoskeletal changes and affects cell migration pathways in the brain. Neurobiol. Dis. 50, 107-119.
20. Koike, M., Nakanishi, H., Saftig, P., Ezaki, J., Isahara, K., Ohsawa, Y., Schulz-Schaeffer, W., Watanabe, T., Waguri, S., Kametaka, S. et al. (2000). Cathepsin D deficiency induces lysosomal storage with ceroid lipofuscin in mouse CNS neurons. J. Neurosci. 20, 6898-6906.
21. Kollmann, K., Damme, M., Markmann, S., Morelle, W., Schweizer, M., Hermans-Borgmeyer, I., Röchert, A. K., Pohl, S., Lübke, T., Michalski, J.-C. et al. (2012). Lysosomal dysfunction causes neurodegeneration in mucolipidosis II 'knock-in' mice. Brain 135, 2661-2675.
22. Konyukh, M., Delorme, R., Chaste, P., Leblond, C., Lemière, N., Nygren, G., Anckarsäter, H., Rastam, M., Ståhlberg, O., Amsellem, F. et al. (2011). Variations of the candidate SEZ6L2 gene on Chromosome 16p11.2 in patients with autism spectrum disorders and in human populations. PLoS ONE 6, e17289.
23. Kornfeld, S. and Sly, W. S. (2000). I-cell disease and pseudo-Hurler polydystrophy: disorders of lysosomal enzyme phosphorylation and localization. In The Metabolic and Molecular Bases of Inherited Disease (ed. C. R. Schriver, A. L. Baudet, W. S. Sly and D. Valle), pp. 3469-3483. New York: McGraw-Hill.
24. Kuhn, P.-H., Koroniak, K., Hogl, S., Colombo, A., Zeitschel, U., Willem, M., Volbracht, C., Schepers, U., Imhof, A., Hoffmeister, A. et al. (2012). Secretome protein enrichment identifies physiological BACE1 protease substrates in neurons. EMBO J. 31, 3157-3168.
25. Kumar, R. A., Marshall, C. R., Badner, J. A., Babatz, T. D., Mukamel, Z., Aldinger, K. A., Sudi, J., Brune, C.W., Goh, G., Karamohamed, S. et al. (2009). Association and mutation analyses of 16p11.2 autism candidate genes. PLoS ONE 4, e4582.
26. Larsson, C. (2006). Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal. 18, 276-284.
27. Laurent-Matha, V., Derocq, D., Prébois, C., Katunuma, N. and Liaudet-Coopman, E. (2006). Processing of human cathepsin D is independent of its catalytic function and auto-activation: involvement of cathepsins L and B. J. Biochem. 139, 363-371.
28. Lefrancois, S., Zeng, J., Hassan, A. J., Canuel, M. and Morales, C. R. (2003). The lysosomal trafficking of sphingolipid activator proteins (SAPs) is mediated by sortilin. EMBO J. 22, 6430-6437.
29. Lindner, R. (2006). Purification of clathrin-coated vesicles from bovine brain, liver, and adrenal gland. In Cell Biology, A Laboratory Handbook, 3rd edn (ed. J. E. Celis), pp. 51-56. Amsterdam, Netherlands: Elsevier.
30. Ludwig, T., Munier-Lehmann, H., Bauer, U., Hollinshead, M., Ovitt, C., Lobel, P. and Hoflack, B. (1994). Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J. 13, 3430-3437.
31. Markmann, S., Thelen, M., Cornils, K., Schweizer, M., Brocke-Ahmadinejad, N., Willnow, T., Heeren, J., Gieselmann, V., Braulke, T. and Kollmann, K. (2015). Lrp1/LDL receptor play critical roles in mannose 6-phosphate-independent lysosomal enzyme targeting. Traffic 16, 743-759.
32. Miñana, M. D., Felipo, V. and Grisolía, S. (1990). Inhibition of protein kinase C induces differentiation in Neuro-2a cells. Proc. Natl. Acad. Sci. USA 87, 4335-4339.
33. Miyazaki, T., Hashimoto, K., Uda, A., Sakagami, H., Nakamura, Y., Saito, S.-Y., Nishi, M., Kume, H., Tohgo, A., Kaneko, I. et al. (2006). Disturbance of cerebellar synaptic maturation in mutant mice lacking BSRPs, a novel brainspecific receptor-like protein family. FEBS Lett. 580, 4057-4064.
34. Mulley, J. C., Iona, X., Hodgson, B., Heron, S. E., Berkovic, S. F., Scheffer, I. E. and Dibbens, L. M. (2011). The role of seizure-related SEZ6 as a susceptibility gene in febrile seizures. Neurol. Res. Int. 2011, 917565.
35. Pohl, S., Tiede, S., Marschner, K., Encarnação, M., Castrichini, M., Kollmann, K., Muschol, N., Ullrich, K., Müller-Loennies, S. and Braulke, T. (2010). Proteolytic processing of the gamma-subunit is associated with the failure to form GlcNAc-1-phosphotransferase complexes and mannose 6-phosphate residues on lysosomal enzymes in human macrophages. J. Biol. Chem. 285, 23936-23944.
36. Pohlmann, R., Boeker, M. W. C. and von Figura, K. (1995). The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J. Biol. Chem. 270, 27311-27318.
37. Reczek, D., Schwake, M., Schröder, J., Hughes, H., Blanz, J., Jin, X., Brondyk, W., Van Patten, S., Edmunds, T. and Saftig, P. (2007). LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of betaglucocerebrosidase. Cell 131, 770-783.
38. Rijnboutt, S., Kal, A. J., Geuze, H. J., Aerts, H. and Strous, G. J. (1991). Mannose 6-phosphate-independent targeting of cathepsin D to lysosomes in HepG2 cells. J. Biol. Chem. 266, 23586-23592.
39. Rijnboutt, S., Stoorvogel, W., Geuze, H. J. and Strous, G. J. (1992). Identification of subcellular compartments involved in biosynthetic processing of cathepsin D. J. Biol. Chem. 267, 15665-15672.
40. 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. (2009). A gene network regulating lysosomal biogenesis and function. Science 24, 473-477.
41. Sevlever, D., Jiang, P. and Yen, S.-H. C. (2008). Cathepsin D is the main lysosomal enzyme involved in the degradation of alpha-synuclein and generation of its carboxy-terminally truncated species. Biochemistry 47, 9678-9687.
42. Shea, T. B., Cressman, C. M., Spencer, M. J., Beermann, M. L. and Nixon, R. A. (1995). Enhancement of neurite outgrowth following calpain inhibition is mediated by protein kinase C. J. Neurochem. 65, 517-527.
43. Siintola, E., Partanen, S., Stromme, P., Haapanen, A., Haltia, M., Maehlen, J., Lehesjoki, A.-E. and Tyynela, J. (2006). Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis. Brain 129, 1438-1445.
44. Slot, J. W. and Geuze, H. J. (2007). Cryosectioning and immunolabeling. Nat. Protoc. 2, 2480-2491.
45. Steinfeld, R., Reinhardt, K., Schreiber, K., Hillebrand, M., Kraetzner, R., Bruck, W., Saftig, P. and Gartner, J. (2006). Cathepsin D deficiency is associated with a human neurodegenerative disorder. Am. J. Hum. Genet. 78, 988-998.
46. Stützer, I., Selevsek, N., Esterházy, D., Schmidt, A., Aebersold, R. and Stoffel, M. (2013). Systematic proteomic analysis identifies β-site amyloid precursor protein cleaving enzyme 2 and 1 (BACE2 and BACE1) substrates in pancreatic β-cells. J. Biol. Chem. 288, 10536-10547.
47. Tyynelä, J., Sohar, I., Sleat, D. E., Gin, R. M., Donnelly, R. J., Baumann, M., Haltia, M. and Lobel, P. (2000). A mutation in the ovine cathepsin D gene causes a congenital lysosomal storage disease with profound neurodegeneration. EMBO J. 19, 2786-2792.
48. van Meel, E., Boonen, M., Zhao, H., Oorschot, V., Ross, F. P., Kornfeld, S. and Klumperman, J. (2011). Disruption of the Man-6-P targeting pathway in mice impairs osteoclast secretory lysosome biogenesis. Traffic 12, 912-924.
49. Wähe, A., Kasmapour, B., Schmaderer, C., Liebl, D., Sandhoff, K., Nykjaer, A., Griffiths, G. and Gutierrez, M. G. (2010). Golgi-to-phagosome transport of acid sphingomyelinase and prosaposin is mediated by sortilin. J. Cell Sci. 123, 2502-2511.
50. Xu, C., Mullersman, J. E., Wang, L., Bin Su, B., Mao, C., Posada, Y., Camarillo, C., Mao, Y., Escamilla, M. A. and Wang, K.-S. (2013). Polymorphisms in seizure 6-like gene are associated with bipolar disorder I: evidence of gene×gender interaction. J. Affect. Disord. 145, 95-99.
51. Yaguchi, H., Yabe, I., Takahashi, H., Okumura, F., Takeuchi, A., Horiuchi, K., Kano, T., Kanda, A., Saito, W., Matsumoto, M. et al. (2014). Identification of anti-SEZ6L2 antibody in a patient with cerebellar ataxia and retinopathy. J. Neurol. 261, 224-226.
52. Yu, Z.-L., Jiang, J.-M., Wu, D.-H., Xie, H.-J., Jiang, J.-J., Zhou, L., Peng, L. and Bao, G.-S. (2007). Febrile seizures are associated with mutation of seizurerelated (SEZ) 6, a brain-specific gene. J. Neurosci. Res. 85, 166-172.