Cathepsin X is secreted by human osteoblasts, digests CXCL-12 and impairs adhesion of hematopoietic stem and progenitor cells to osteoblasts

Haematologica

Volumn 95, Issue 9, 2010, Pages 1452-1460

  Staudt, Nicole D ^a   Aicher, Wilhelm K ^a   Kalbacher, Hubert ^b   Stevanovic, Stefan ^c   Carmona, Adriana K ^d   Bogyo, Matthew ^e   Klein, Gerd ^a  

^a Center for Medical Research   (Germany)

^b Medical and Natural Sciences Research Center   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Active site labeling; Cell adhesion; Cysteine cathepsins; Proteases; Proteolytic microenvironment; Stem cell niche

Indexed keywords

CATHEPSIN X; EXOPEPTIDASE; STROMAL CELL DERIVED FACTOR 1;

ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME SUBSTRATE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; OSTEOBLAST; PROTEIN EXPRESSION; STROMA CELL; SUPERNATANT; WESTERN BLOTTING;

BONE MARROW; CATHEPSIN Z; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; HEMATOPOIETIC STEM CELLS; HUMANS; OSTEOBLASTS;

EID: 77956832357     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2009.018671     Document Type: Article

References (40)

1. Santamaria I, Velasco G, Pendas AM, Fueyo A, Lopez-Otin C. Cathepsin Z, a novel human cysteine proteinase with a short propeptide domain and a unique chromosomal location. J Biol Chem. 1998;273(27):16816-16823.
2. Nagler DK, Menard R. Human cathepsin X: a novel cysteine protease of the papain family with a very short proregion and unique insertions. FEBS Lett. 1998;434(1-2):135-139.
3. Turk V, Turk B, Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001;20(17):4629-4633.
4. Brix K, Dunkhorst A, Mayer K, Jordans S. Cysteine cathepsins: cellular roadmap to different functions. Biochimie. 2008; 90(2):194-207.
5. Goulet B, Baruch A, Moon NS, Poirier M, Sansregret LL, Erickson A, et al. A cathepsin L isoform that is devoid of a signal peptide localizes to the nucleus in S phase and processes the CDP/Cux transcription factor. Mol Cell. 2004;14(2):207-219.
6. Mohamed MM, Sloane BF. Cysteine cathepsins: multifunctional enzymes in cancer. Nat Rev Cancer. 2006;6(10):764-775.
7. Nagler DK, Zhang R, Tam W, Sulea T, Purisima EO, Menard R. Human cathepsin X: a cysteine protease with unique carboxypeptidase activity. Biochemistry. 1999;38(39):12648-12654.
8. Lechner AM, Assfalg-Machleidt I, Zahler S, Stoeckelhuber M, Machleidt W, Jochum M, et al. RGD-dependent binding of procathepsin X to integrin alphavbeta3 mediates cell-adhesive properties. J Biol Chem. 2006;281(51):39588-39597.
9. Puzer L, Cotrin SS, Cezari MH, Hirata IY, Juliano MA, Stefe I, et al. Recombinant human cathepsin X is a carboxymonopeptidase only: a comparison with cathepsins B and L. Biol Chem. 2005;386(11):1191-1195.
10. Kos J, Sekirnik A, Premzl A, Zavasnik Bergant V, Langerholc T, Turk B, et al. Carboxypeptidases cathepsins X and B display distinct protein profile in human cells and tissues. Exp Cell Res. 2005;306(1):103-113.
11. Jevnikar Z, Obermajer N, Bogyo M, Kos J. The role of cathepsin X in the migration and invasiveness of T lymphocytes. J Cell Sci. 2008;121(Pt 16):2652-2661.
12. Nagler DK, Kruger S, Kellner A, Ziomek E, Menard R, Buhtz P, et al. Up-regulation of cathepsin X in prostate cancer and prostatic intraepithelial neoplasia. Prostate. 2004;60(2):109-119.
13. Buhling F, Peitz U, Kruger S, Kuster D, Vieth M, Gebert I, et al. Cathepsins K, L, B, X and W are differentially expressed in normal and chronically inflamed gastric mucosa. Biol Chem. 2004;385(5):439-445.
14. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol. 2006;6(2):93-106.
15. Scadden DT. The stem-cell niche as an entity of action. Nature. 2006;441(7097): 1075-1079.
16. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425(6960):841-846.
17. Zhang J, Niu C, Ye L, Huang H, He X, Tong W-G, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425 (6960):836-841.
18. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature. 2009;457(7225):92-96.
19. Broxmeyer HE. Chemokines in hematopoiesis. Curr Opin Hematol. 2008;15(1):49-58.
20. Shirozu M, Nakano T, Inazawa J, Tashiro K, Tada H, Shinohara T, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics. 1995;28(3):495-500.
21. Lapidot T, Kollet O. The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immunedeficient NOD/SCID and NOD/SCID/ B2m(null) mice. Leukemia. 2002;16(10): 1992-2003.
22. Marquez-Curtis L, Jalili A, Deiteren K, Shirvaikar N, Lambeir AM, Janowska- Wieczorek A. Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of stromal cell-derived factor-1alpha: another player in hematopoietic stem/progenitor cell mobilization? Stem Cells. 2008;26(5):1211-1220.
23. Vagima Y, Avigdor A, Goichberg P, Shivtiel S, Tesio M, Kalinkovich A, et al. MT1- MMP and RECK are involved in human CD34+ progenitor cell retention, egress, and mobilization. J Clin Invest. 2009; 119(3):492-503.
24. Nervi B, Link DC, DiPersio JF. Cytokines and hematopoietic stem cell mobilization. J Cell Biochem. 2006;99(3):690-705.
25. Levesque JP, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C, et al. Characterization of hematopoietic progen itor mobilization in protease-deficient mice. Blood. 2004;104(1):65-72.
26. Greenbaum D, Medzihradszky KF, Burlingame A, Bogyo M. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem Biol. 2000;7(8):569-581.
27. Pungercar JR, Caglic D, Sajid M, Dolinar M, Vasiljeva O, Pozgan U, et al. Autocatalytic processing of procathepsin B is triggered by proenzyme activity. FEBS J. 2009; 276(3):660-668.
28. Aisa MC, Beccari T, Costanzi E, Maggio D. Cathepsin B in osteoblasts. Biochim Biophys Acta. 2003;1621(2):149-159.
29. Obermajer N, Premzl A, Zavasnik Bergant T, Turk B, Kos J. Carboxypeptidase cathepsin X mediates beta2-integrin-dependent adhesion of differentiated U-937 cells. Exp Cell Res. 2006;312(13):2515-2527.
30. Grote K, Salguero G, Ballmaier M, Dangers M, Drexler H, Schieffer B. The angiogenic factor CCN1 promotes adhesion and migration of circulating CD34+ progenitor cells: potential role in angiogenesis and endothelial regeneration. Blood. 2007; 110(3):877-885.
31. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002;3(7):687-694.
32. Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest. 2003;111(2):187-96.
33. Christopher MJ, Liu F, Hilton MJ, Long F, Link DC. Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokineinduced mobilization. Blood. 2009;114(7): 1331-1339.
34. Neiva K, Sun YX, Taichman RS. The role of osteoblasts in regulating hematopoietic stem cell activity and tumor metastasis. Braz J Med Biol Res. 2005;38(10):1449-1454.
35. McQuibban GA, Butler GS, Gong JH, Bendall L, Power C, Clark-Lewis I, et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cellderived factor-1. J Biol Chem. 2001; 276(47):43503-43508.
36. Lambeir AM, Proost P, Durinx C, Bal G, Senten K, Augustyns K, et al. Kinetic investigation of chemokine truncation by CD26/dipeptidyl peptidase IV reveals a striking selectivity within the chemokine family. J Biol Chem. 2001;276(32):29839-29845.
37. Valenzuela-Fernandez A, Planchenault T, Baleux F, Staropoli I, Le-Barillec K, Leduc D, et al. Leukocyte elastase negatively regulates stromal cell-derived factor-1 (SDF- 1)/CXCR4 binding and functions by amino-terminal processing of SDF-1 and CXCR4. J Biol Chem. 2002;277(18):15677-15689.
38. Delgado MB, Clark-Lewis I, Loetscher P, Langen H, Thelen M, Baggiolini M, et al. Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes. Eur J Immunol. 2001;31(3): 699-707.
39. Caglic D, Pungercar JR, Pejler G, Turk V, Turk B. Glycosaminoglycans facilitate procathepsin B activation through disruption of propeptide-mature enzyme interactions. J Biol Chem. 2007;282(45):33076-33085.
40. Nascimento FD, Rizzi CC, Nantes IL, Stefe I, Turk B, Carmona AK, et al. Cathepsin X binds to cell surface heparan sulfate proteoglycans. Arch Biochem Biophys. 2005; 436(2):323-332.