Cellular repressor of E1A-stimulated genes is a bona fide lysosomal protein which undergoes proteolytic maturation during its biosynthesis

Experimental Cell Research

Volumn 314, Issue 16, 2008, Pages 3036-3047

  Schähs, Philipp ^a   Weidinger, Petra ^a   Probst, Olivia C ^a   Svoboda, Barbara ^a   Stadlmann, Johannes ^a   Beug, Hartmut ^b   Waerner, Thomas ^b   Mach, Lukas ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

Cathepsin; CREG; Lysosome; Mannose 6 phosphate Protein targeting; Proteolytic maturation

Indexed keywords

CELL PROTEIN; CELLULAR REPRESSOR OF E1A STIMULATED PROTEIN; GREEN FLUORESCENT PROTEIN; LYSOSOME PROTEIN; OLIGOSACCHARIDE; RECOMBINANT PROTEIN; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; EMBRYO; FIBROBLAST; GENE CONSTRUCT; GENE FUSION; IMMUNOLOCALIZATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS;

EID: 51649110079     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.06.015     Document Type: Article

References (41)

1. Veal E., Eisenstein M., Tseng Z.H., and Gill G. A cellular repressor of E1A-stimulated genes that inhibits activation by E2F. Mol. Cell. Biol. 18 (1998) 5032-5041
2. Veal E., Groisman R., Eisenstein M., and Gill G. The secreted glycoprotein CREG enhances differentiation of NTERA-2 human embryonal carcinoma cells. Oncogene 19 (2000) 2120-2128
3. Xu L., Liu J.-M., and Chen L.-Y. CREG, a new regulator of ERK1/2 in cardiac hypertrophy. J. Hypertens. 22 (2004) 1579-1587
4. Gordon P.V., Paxton J.B., and Fox N.S. The cellular repressor of E1A-stimulated genes mediates glucocorticoid-induced loss of the type-2 IGF receptor in ileal epithelial cells. J. Endocrinol. 185 (2005) 265-273
5. Di Bacco A., and Gill G. The secreted glycoprotein CREG inhibits cell growth dependent on the mannose 6-phosphate/insulin-like growth factor II receptor. Oncogene 22 (2003) 5436-5445
6. Journet A., Chapel A., Kieffer S., Louwagie M., Luche S., and Garin J. Towards a human repertoire of monocytic lysosomal proteins. Electrophoresis 21 (2000) 3411-3419
7. Journet A., Chapel A., Kieffer S., Roux F., and Garin J. Proteomic analysis of human lysosomes: application to monocytic and breast cancer cells. Proteomics 2 (2002) 1026-1040
8. Sleat D.E., Lackland H., Wang Y., Sohar I., Xiao G., Li H., and Lobel P. The human brain mannose 6-phosphate glycoproteome: a complex mixture composed of multiple isoforms of many soluble lysosomal proteins. Proteomics 5 (2005) 1520-1532
9. Kollmann K., Mutenda K.E., Balleininger M., Eckermann E., von Figura K., Schmidt B., and Lübke T. Identification of novel lysosomal matrix proteins by proteome analysis. Proteomics 5 (2005) 3966-3978
10. Sleat D.E., Zheng H., Qian M., and Lobel P. Identification of sites of mannose 6-phosphorylation on lysosomal proteins. Mol. Cell. Proteomics 5 (2006) 686-701
11. Qian M., Sleat D.E., Zheng H., Moore D., and Lobel P. Proteomic analysis of serum from mutant mice reveals lysosomal proteins selectively transported by each of the two mannose 6-phosphate receptors. Mol. Cell. Proteomics 7 (2008) 58-70
12. Sacher M., Di Bacco A., Lunin V.V., Ye Z., Wagner J., Gill G., and Cygler M. The crystal structure of CREG, a secreted glycoprotein involved in cellular growth and differentiation. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 18326-18331
13. von Figura K., and Hasilik A. Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55 (1986) 167-193
14. Kornfeld S., and Mellman I. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5 (1989) 483-525
15. Ghosh P., Dahms N.M., and Kornfeld S. Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell Biol. 4 (2003) 202-212
16. Pohlmann R., Wendland M., Boeker C., and von Figura K. The two mannose 6-phosphate receptors transport distinct complements of lysosomal proteins. J. Biol. Chem. 270 (1995) 27311-27318
17. Mach L., Schwihla H., Stüwe K., Rowan A.D., Mort J.S., and Glössl J. Activation of procathepsin B in human hepatoma cells: the conversion into the mature enzyme relies on the action of cathepsin B itself. Biochem. J. 293 (1993) 437-442
18. Mach L., Stüwe K., Hagen A., Ballaun C., and Glössl J. Proteolytic processing of cathepsin B. The role of the primary structure of the latent precursor and of the carbohydrate moiety for cell-type-specific molecular forms of the enzyme. Biochem. J. 282 (1992) 577-582
19. Kasper D., Dittmer F., von Figura K., and Pohlmann R. Neither type of mannose 6-phosphate receptor is sufficient for targeting of lysosomal enzymes along intracellular routes. J. Cell Biol. 134 (1996) 615-623
20. Dennes A., Cromme C., Suresh K., Kumar N.S., Eble J.A., Hahnenkamp A., and Pohlmann R. The novel Drosophila lysosomal enzyme receptor protein mediates lysosomal sorting in mammalian cells and binds mammalian and Drosophila GGA adaptors. J. Biol. Chem. 280 (2005) 12849-12857
21. Oft M., Peli J., Rudaz C., Schwarz H., Beug H., and Reichmann E. TGF-beta1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev. 10 (1996) 2462-2477
22. Müntener K., Zwicky R., Csucs G., and Baici A. The alternative use of exons 2 and 3 in cathepsin B mRNA controls enzyme trafficking and triggers nuclear fragmentation in human cells. Histochem. Cell Biol. 119 (2003) 93-101
23. Sarkar M., Pagny S., Ünligil U., Joziasse D., Mucha J., Glössl J., and Schachter H. Removal of 106 amino acids from the N-terminus of UDP-GlcNAc:a-3-d-mannoside b-1,2-N-acetylglucosaminyl-transferase I does not inactivate the enzyme. Glycoconj. J. 15 (1998) 193-197
24. Schmid J.A., Mach L., Paschke E., and Glössl J. Accumulation of sialic acid in endocytic compartments interferes with the formation of mature lysosomes. J. Biol. Chem. 274 (1999) 19063-19071
25. Storrie B., and Madden E.A. Isolation of subcellular organelles. Meth. Enzymol. 182 (1990) 203-225
26. Rome L.H., Garvin A.J., Allietta M.M., and Neufeld E.F. Two species of lysosomal organelles in cultured human fibroblasts. Cell 17 (1979) 143-153
27. Coulibaly S., Schwihla H., Abrahamson M., Albini A., Cerni C., Clark J.L., Ng K.M., Katunuma N., Schlappack O., Glössl J., and Mach L. Modulation of invasive properties of murine squamous carcinoma cells by heterologous expression of cathepsin B and cystatin C. Int. J. Cancer 83 (1999) 526-531
28. Kolarich D., Leonard R., Hemmer W., and Altmann F. The N-glycans of yellow jacket venom hyaluronidases and the protein sequence of its major isoform in Vespula vulgaris. FEBS J. 272 (2005) 5182-5190
29. Mach L. Biosynthesis of lysosomal proteinases in health and disease. Biol. Chem. 383 (2002) 751-756
30. Braulke T., Geuze H.J., Slot J.W., Hasilik A., and von Figura K. On the effects of weak bases and monensin on sorting and processing of lysosomal enzymes in human cells. Eur. J. Cell Biol. 43 (1987) 316-321
31. Kornfeld R., and Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54 (1985) 631-664
32. Jongen S.P., Gerwig G.J., Leeflang B.R., Koles K., Mannesse M.L., van Berkel P.H., Pieper F.R., Kroos M.A., Reuser A.J., Zhou Q., Jin X., Zhang K., Edmunds T., and Kamerling J.P. N-glycans of recombinant human acid alpha-glucosidase expressed in the milk of transgenic rabbits. Glycobiology 17 (2007) 600-619
33. Probst O.C., Ton P., Svoboda B., Gannon A., Schuhmann W., Wieser J., Pohlmann R., and Mach L. The 46-kDa mannose 6-phosphate receptor does not depend on endosomal acidification for delivery of hydrolases to lysosomes. J. Cell Sci. 119 (2006) 4935-4943
34. Abrahamson M., Mason R.W., Hansson H., Buttle D.J., Grubb A., and Ohlsson K. Human cystatin C. Role of the N-terminal segment in the inhibition of human cysteine proteinases and in its inactivation by leucocyte elastase. Biochem. J. 273 (1991) 621-626
35. Murata M., Miyashita S., Yokoo C., Tamai M., Hanada K., Hatayama K., Towatari T., Nikawa T., and Katunuma N. Novelepoxysuccinyl peptides. Selective inhibitors of cathepsin B, in vitro. FEBS Lett. 280 (1991) 307-310
36. Kunita R., Otomo A., and Ikeda J.-E. Identification and characterization of novel members of the CREG family, putative secreted glycoproteins expressed specifically in brain. Genomics 80 (2002) 456-460
37. r 46 000 mannose 6-phosphate receptor: its role in targeting of lysosomal enzymes. EMBO J. 6 (1987) 2677-2681
38. Wang X.Q., Fung M.R., Barlow D.P., and Wagner E.F. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372 (1994) 464-467
39. Brogiolo W., Stocker H., Ikeya T., Rintelen F., Fernandez R., and Hafen E. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11 (2001) 213-221
40. Aeed P.A., and Elhammer A.P. Glycosylation of recombinant prorenin in insect cells: the insect cell line Sf9 does not express the mannose 6-phosphate recognition signal. Biochemistry 33 (1994) 8793-8797
41. Futerman A.H., and van Meer G. The cell biology of lysosomal storage diseases. Nat. Rev. Mol. Cell Biol. 5 (2004) 554-565