Glycosylation directs targeting and activation of cystatin F from intracellular and extracellular sources

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Volumn 10, Issue 4, 2009, Pages 425-437

  Colbert, Jeff D ^a   Plechanovová, Anna ^a   Watts, Colin ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Cathepsin C; Cystatin; Endocytosis internalization; Glycosylation; Mannose 6 phosphate

Indexed keywords

CYSTATIN; CYSTATIN F; MANNOSE 6 PHOSPHATE; OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL SECRETION; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN TARGETING; TRANSPORT KINETICS;

AMINO ACID SEQUENCE; ANIMALS; ASPARAGINE; CELL LINE; CYSTATINS; DIMERIZATION; ENDOSOMES; GLYCOSYLATION; HUMANS; MANNOSEPHOSPHATES; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OLIGOSACCHARIDES; PROTEIN CONFORMATION; TUMOR MARKERS, BIOLOGICAL;

EID: 63049116236     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00881.x     Document Type: Article

References (48)

1. Abrahamson M, Alvarez-Fernandez M, Nathanson CM. Cystatins. Biochem Soc Symp 2003; 70: 179-199.
2. Kopitar-Jerala N. The role of cystatins in cells of the immune system. FEBS Lett 2006; 580: 6295-6301.
3. Zeeuwen PL, van Vlijmen-Willems IM, Hendriks W, Merkx GF, Schalkwijk J. A null mutation in the cystatin M/E gene of ichq mice causes juvenile lethality and defects in epidermal cornification. Hum Mol Genet 2002; 11: 2867-2875.
4. Bode W, Engh R, Musil D, Thiele U, Huber R, Karshikov A, Brzin J, Kos J, Turk V. The 2.0 A X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J 1988; 7: 2593-2599.
5. Stubbs MT, Laber B, Bode W, Huber R, Jerala R, Lenarcic B, Turk V. The refined 2.4 A X-ray crystal structure of recombinant human stefin B in complex with the cysteine proteinase papain: A novel type of proteinase inhibitor interaction. EMBO J 1990; 9: 1939-1947.
6. Jenko S, Dolenc I, Guncar G, Dobersek A, Podobnik M, Turk D. Crystal structure of Stefin A in complex with cathepsin H: N-terminal residues of inhibitors can adapt to the active sites of endo- and exopeptidases. J Mol Biol 2003; 326: 875-885.
7. Alvarez-Fernandez M, Barrett AJ, Gerhartz B, Dando PM, Ni J, Abrahamson M. Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site. J Biol Chem 1999; 272: 19195-19203.
8. Halfon S, Ford J, Foster J, Dowling L, Lucian L, Sterling M, Xu Y, Weiss M, Ikeda M, Liggett D, Helms A, Caux C, Lebecque S, Hannum C, Menon S et al. Leukocystatin, a new Class II cystatin expressed selectively by hematopoietic cells. J Biol Chem 1998; 273: 16400-16408.
9. Ni J, Fernandez A, Danielsson L, Chillakuru RA, Zhang J, Grub A, Su J, Gentz R, Abrahamson M. Cystatin F is a glycosylated human low molecular weight cystein proteinase inhibitor. J Biol Chem 1998; 273: 24797-24804.
10. Cappello F, Gatti E, Camossetto V, David A, Lelouard H, Pierre P. Cystatin F is secreted, but artificial modification of its C-terminus can induce its endocytic targeting. Exp Cell Res 2004; 297: 607-618.
11. Langerholc T, Zavasnik-Bergant V, Turk B, Turk V, Abrahamson M, Kos J. Inhibitory properties of cystatin F and its localization in U937 promonocyte cells. The FEBS J 2005; 272: 1535-1545.
12. Schuettelkopf AW, Hamilton G, Watts C, van Aalten DM. Structural basis of reduction-dependent activation of human cystatin F. J Biol Chem 2006; 281: 16570-16575.
13. Nathanson CM, Wasselius J, Wallin H, Abrahamson M. Regulated expression and intracellular localization of cystatin F in human U937 cells. Eur J Biochem 2002; 269: 5502-5511.
14. Taupin P, Ray J, Fischer WH, Suhr ST, Hakansson K, Grubb A, Gage FH. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 2000; 28: 385-397.
15. Dahl A, Eriksson PS, Davidsson P, Persson AI, Ekman R, Westman-Brinkmalm A. Demonstration of multiple novel glycoforms of the stem cell survival factor CCg. J Neurosci Res 2004; 77: 9-14.
16. Hamilton G, Colbert JD, Schuettelkopf AW, Watts C. Cystatin F is a cathepsin C-directed protease inhibitor regulated by proteolysis. EMBO J 2008; 27: 499-508.
17. Pham CT, Ley TJ. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc Natl Acad Sci U S A 1999; 96: 8627-8632.
18. Adkison AM, Raptis SZ, Kelley DG, Pham CT. Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J Clin Invest 2002; 109: 363-371.
19. Wolters PJ, Pham CT, Muilenburg DJ, Ley TJ, Caughey GH. Dipeptidyl peptidase I is essential for activation of mast cell chymases, but not tryptases, in mice. J Biol Chem 2001; 276: 18551-18556.
20. Sato C, Kim JH, Abe Y, Saito K, Yokoyama S, Kohda D. Characterization of the N-oligosaccharides attached to the atypical Asn-X-Cys sequence of recombinant human epidermal growth factor receptor. J Biochem 2000; 127: 65-72.
21. Vance BA, Wu W, Ribaudo RK, Segal DM, Kearse KP. Multiple dimeric forms of human CD69 result from differential addition of N-glycans to typical (Asn-X-Ser/Thr) and atypical (Asn-X-cys) glycosylation motifs. J Biol Chem 1997; 272: 23117-23122.
22. Ghosh P, Dahms NM, Kornfeld S. Mannose 6-phosphate receptors: New twists in the tale. Nature Rev Mol Cell Biol 2003; 4: 202-212.
23. Warfel AH, Zucker-Franklin D, Frangione B, Ghiso J. Constitutive secretion of cystatin C (gamma-trace) by monocytes and macrophages and its downregulation after stimulation. J Ex Med 1987; 166: 1912-1917.
24. Isemura S, Saitoh E, Sanada K, Minakata K. Identification of full-sized forms of salivary (S-type) cystatins (cystatin SN, cystatin SA, cystatin S, and two phosphorylated forms of cystatin S) in human whole saliva and determination of phosphorylation sites of cystatin S. J Biochem 1991; 110: 648-654.
25. Balbin M, Hall A, Grubb A, Mason RW, Lopez-Otin C, Abrahamson M. Structural and functional characterization of two allelic variants of human cystatin D sharing a characteristic inhibition spectrum against mammalian cysteine proteinases. J Biol Chem 1994; 269: 23156-23162.
26. Reddy VY, Zhang QY, Weiss SJ. Pericellular mobilization of the tissue-destructive cysteine proteinases, cathepsins B, L, and S, by human monocyte-derived macrophages. Proc Natl Acad Sci U S A 1995; 92: 3849-3853.
27. Linebaugh BE, Sameni M, Day NA, Sloane BF, Keppler D. Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur J Bicoem 1999; 264: 100-109.
28. Shi GP, Munger JS, Meara JP, Rich DH, Chapman HA. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J Biol Chem 1992; 267: 7258-7262.
29. Zeeuwen PL, Ishida-Yamamoto A, van Vlijmen-Willems IM, Cheng T, Bergers M, Iizuka H, Schalkwijk J. Colocalization of cystatin M/E and cathepsin V in lamellar granules and corneodesmosomes suggests a functional role in epidermal differentiation. J Invest Derm 2007; 127: 120-128.
30. Journet A, Chapel A, Kieffer S, Louwagie M, Luche S, Garin J. Towards a human repertoire of monocytic lysosomal proteins. Electrophoresis 2000; 21: 3411-3419.
31. Dittmer F, Ulbrich EJ, Hafner A, Schmahl W, Meister T, Pohlmann R, von Figura K. Alternative mechanisms for trafficking of lysosomal enzymes in mannose 6-phosphate receptor-deficient mice are cell type-specific. J Cell Sci 1999; 112: 1591-1597.
32. Nielsen MS, Madsen P, Christensen EI, Nykjaer A, Gliemann J, Kasper D, Pohlmann R, Petersen CM. The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J 2001; 20: 2180-2190.
33. Grinnell BW, Walls JD, Gerlitz B. Glycosylation of human protein C affects its secretion, processing, functional activities, and activation by thrombin. J Biol Chem 1991; 266: 9778-9785.
34. Sando GN, Neufeld EF. Recognition and receptor-mediated uptake of a lysosomal enzyme, alpha-l-iduronidase, by cultured human fibroblasts. Cell 1977; 12: 619-627.
35. York SJ, Arneson LS, Gregory WT, Dahms NM, Kornfeld S. The rate of internalization of the mannose 6-phosphate/insulin-like growth factor II receptor is enhanced by multivalent ligand binding. J Biol Chem 1999; 274: 1164-1171.
36. Nielsen R, Courtoy PJ, Jacobsen C, Dom G, Lima WR, Jadot M, Willnow TE, Devuyst O, Christensen EI. Endocytosis provides a major alternative pathway for lysosomal biogenesis in kidney proximal tubular cells. Proc Natl Acad Sci U S A 2007; 104: 5407-5412.
37. Kaseda R, Iino N, Hosojima M, Takeda T, Hosaka K, Kobayashi A, Yamamoto K, Suzuki A, Kasai A, Suzuki Y, Gejyo F, Saito A. Megalin-mediated endocytosis of cystatin C in proximal tubule cells. Biochem Biophys Res Commun 2007; 357: 1130-1134.
38. Ullrich K, von Figura K. Endocytosis of beta-N-acetylglucosaminidase from sections of mucolipidosis-II and-III fibroblasts by non-parenchymal rat liver cells. Biochem J 1979; 182: 245-247.
39. Ullrich K, Basner R, Gieselmann V, Von Figura K. Recognition of human urine alpha-N-acetylglucosaminidase by rat hepatocytes. Involvement of receptors specific for galactose, mannose 6-phosphate and mannose. Biochem J 1979; 180: 413-419.
40. Stahl P, Gordon S. Expression of a mannosyl-fucosyl receptor for endocytosis on cultured primary macrophages and their hybrids. J Cell Biol 1982; 93: 49-56.
41. Toyama-Sorimachi N, Kitamura F, Habuchi H, Tobita Y, Kimata K, Miyasaka M. Widespread expression of chondroitin sulfate-type serglycins with CD44 binding ability in hematopoietic cells. J Biol Chem 1997; 272: 26714-26719.
42. Harris EN, Weigel JA, Weigel PH. The human hyaluronan receptor for endocytosis (HARE/Stabilin-2) is a systemic clearance receptor for heparin. J Biol Chem 2008; 283: 17341-17350.
43. Grubb A, Lofberg H. Human gamma-trace, a basic microprotein: Amino acid sequence and presence in the adenohypophysis. Proc Natl Acad Sci U S A 1982; 79: 3024-3027.
44. Ekstrom U, Wallin H, Lorenzo J, Holmqvist B, Abrahamson M, Aviles FX. Internalization of cystatin C in human cell lines. FEBS J 2008; 275: 4571-4582.
45. Honey K, Benlagha K, Beers C, Forbush K, Teyton L, Kleijmeer MJ, Rudensky AY, Bendelac A. Thymocyte expression of cathepsin L is essential for NKT cell development. Nature Immunol 2002; 3: 1069-1074.
46. Kasper D, Dittmer F, von Figura K, Pohlmann R. Neither type of mannose 6-phosphate receptor is sufficient for targeting of lysosomal enzymes along intracellular routes. J Cell Biol 1996; 134: 615-623.
47. West MA, Wallin RP, Matthews SP, Svensson HG, Zaru R, Ljunggren HG, Prescott AR, Watts C. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 2004; 305: 1153-1157.
48. Siegel LM, Monty KJ. Determination of molecular weights and frictional ratios of proteins in impure systems by use of gel filtration and density gradient centrifugation. Application to crude preparations of sulfite and hydroxylamine reductases. Biochim Biophys Acta 1966; 112: 346-362.