Alginates induce legumain activity in RAW 264.7 cells and accelerate autoactivation of prolegumain

Bioactive Carbohydrates and Dietary Fibre

Volumn 2, Issue 1, 2013, Pages 30-44

  Berven, Lise ^a   Solberg, Rigmor ^a   Truong, Hong Hoa Thi ^a   Arlov, Øystein ^b   Lillelund Aachmann, Finn ^b   Skjåk Bræk, Gudmund ^b   Egge Jacobsen, Wolfgang M ^a   Thidemann Johansen, Harald ^a   Samuelsen, Anne Berit C ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Alginate; Guluronic acid; Legumain; Mannuronic acid; Protease; RAW 264.7 cells

Indexed keywords

ALGINIC ACID; CARBOXYLIC ACID; ENZYME PRECURSOR; HEPARIN; LEGUMAIN; OLIGOMER;

ACCELERATION; ANIMAL CELL; ARTICLE; CHEMICAL INTERACTION; CONFORMATION; DEPOLYMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; IONIC STRENGTH; METASTASIS; MOLECULAR SIZE; MOUSE; NONHUMAN; PH; PINOCYTOSIS; PRIORITY JOURNAL; REDUCTION KINETICS; TUMOR INVASION;

EID: 84886707904     PISSN: 22126198     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcdf.2013.08.003     Document Type: Article

References (44)

1. P.C. Almeida, I.L. Nantes, J.R. Chagas, C.C. Rizzi, A. Faljoni-Alario, and E. Carmona Cathepsin B activity regulation. Heparin-like glycosaminogylcans protect human cathepsin B from alkaline pH-induced inactivation The Journal of Biological Chemistry 276 2 2001 944 951 (Pubitemid 32096513)
2. T. Anthonsen, B. Larsen, and O. Smidsrød NMR-studies of the interaction of metal ions with poly(1,4-hexuronates). II. The binding of europium ions to sodium methyl alpha-d-galactopyranosiduronate Acta Chemica Scandinavica 27 7 1973 2671 2673
3. Arlov O. (2012). Heparin analogs created by sulfation of alginate using a chemoenzymatic strategy. NTNU, Trondheim, Norway: NTNU, Trondheim, Norway.
4. L. Berven, H.T. Johansen, R. Solberg, S.O. Kolset, and A.B. Samuelsen Autoactivation of prolegumain is accelerated by glycosaminoglycans Biochimie 95 4 2013 772 781
5. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Analytical Biochemistry 72 1976 248 254
6. S.C. Chang, J.A. Rowley, G. Tobias, N.G. Genes, A.K. Roy, and D.J. Mooney Injection molding of chondrocyte/alginate constructs in the shape of facial implants Journal of Biomedical Materials Research 55 4 2001 503 511 (Pubitemid 32336280)
7. J.M. Chen, P.M. Dando, N.D. Rawlings, M.A. Brown, N.E. Young, and R.A. Stevens Cloning, isolation, and characterization of mammalian legumain, an asparaginyl endopeptidase The Journal of Biological Chemistry 272 12 1997 8090 8098 (Pubitemid 27137377)
8. J.M. Chen, P.M. Dando, R.A. Stevens, M. Fortunato, and A.J. Barrett Cloning and expression of mouse legumain, a lysosomal endopeptidase The Biochemical Journal 335 Pt 1 1998 111 117 (Pubitemid 28477056)
9. J.H. Cummings, and G.T. Macfarlane The control and consequences of bacterial fermentation in the human colon The Journal of Applied Bacteriology 70 6 1991 443 459
10. E. Dall, and H. Brandstetter Activation of legumain involves proteolytic and conformational events, resulting in a context- and substrate-dependent activity profile Acta Crystallographica Section F: Structural Biology and Crystallization Communications 68 Pt 1 2012 24 31
11. T. Espevik, M. Otterlei, G. Skjåk-Bræk, L. Ryan, S.D. Wright, and A. Sundan The involvement of CD14 in stimulation of cytokine production by uronic acid polymers European Journal of Immunology 23 1 1993 255 261 (Pubitemid 23031925)
12. T. Espevik, A.M. Rokstad, B. Kulseng, B. Strand, and G. Skjåk-Bræk Mechanisms of the most immune response to alginate microcapsules. The Bioartificial Pancreas and Other Biohybrid Therapies 2009 12
13. S. Falcone, E. Cocucci, P. Podini, T. Kirchhausen, E. Clementi, and J. Meldolesi Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events Journal of Cell Science 119 Pt 22 2006 4758 4769 (Pubitemid 44964272)
14. T.H. Flo, L. Ryan, L. Kilaas, G. Skjak-Braek, R.R. Ingalls, and A. Sundan Involvement of CD14 and beta2-integrins in activating cells with soluble and particulate lipopolysaccharides and mannuronic acid polymers Infection and Immunity 68 12 2000 6770 6776 (Pubitemid 32463383)
15. T.H. Flo, L. Ryan, E. Latz, O. Takeuchi, B.G. Monks, and E. Lien Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers The Journal of Biological Chemistry 277 38 2002 35489 35495
16. B. Fremond, C. Malandain, C. Guyomard, C. Chesne, A. Guillouzo, and J.P. Campion Correction of bilirubin conjugation in the Gunn rat using hepatocytes immobilized in alginate gel beads as an extracorporeal bioartificial liver Cell Transplantation 2 6 1993 453 460 (Pubitemid 23336323)
17. J. Gawenda, F. Traub, H.J. Luck, H. Kreipe, and R. von Wasielewski Legumain expression as a prognostic factor in breast cancer patients Breast Cancer Research and Treatment 102 1 2007 1 6 (Pubitemid 46294961)
18. M. Gimmestad, H. Sletta, H. Ertesvag, K. Bakkevig, S. Jain, and S.J. Suh The Pseudomonas fluorescens AlgG protein, but not its mannuronan C-5-epimerase activity, is needed for alginate polymer formation Journal of Bacteriology 185 12 2003 3515 3523 (Pubitemid 36676417)
19. S. Halfon, S. Patel, F. Vega, S. Zurawski, and G. Zurawski Autocatalytic activation of human legumain at aspartic acid residues FEBS Letters 438 1-2 1998 114 118 (Pubitemid 28517846)
20. A.I. Hashim, X. Zhang, J.W. Wojtkowiak, G.V. Martinez, and R.J. Gillies Imaging pH and metastasis NMR in Biomedicine 24 6 2011 582 591
21. R. Huang, Y. Du, and J.H. Yang Preparation and in vitro anticoagulant activities of alginate sulfate and its quaternized derivates Carbohydrate Polymers 52 1 2003 19 24
22. H.T. Johansen, C.G. Knight, and A.J. Barrett Colorimetric and fluorimetric microplate assays for legumain and a staining reaction for detection of the enzyme after electrophoresis Analytical Biochemistry 273 2 1999 278 283 (Pubitemid 29430671)
23. J.B. Kim, and N.C. Carpita Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles Plant Physiology 98 2 1992 646 653
24. Kozlowski L. 2012. Isoelectric point calculator. 〈 http://www.isoelectric.ovh.orgâŒ.
25. M. Kurachi, T. Nakashima, C. Miyajima, Y. Iwamoto, T. Muramatsu, and K. Yamaguchi Comparison of the activities of various alginates to induce TNF-alpha secretion in RAW264.7 cells Journal of Infection and Chemotherapy: Official Journal of the Japan Society of Chemotherapy 11 4 2005 199 203 (Pubitemid 41216453)
26. B. Li, D. Cramer, S. Wagner, R. Hansen, C. King, and S. Kakar Yeast glucan particles activate murine resident macrophages to secrete proinflammatory cytokines via MyD88- and Syk kinase-dependent pathways Clinical Immunology 124 2 2007 170 181 (Pubitemid 47061522)
27. D.N. Li, S.P. Matthews, A.N. Antoniou, D. Mazzeo, and C. Watts Multistep autoactivation of asparaginyl endopeptidase in vitro and in vivo The Journal of Biological Chemistry 278 40 2003 38980 38990 (Pubitemid 37221799)
28. A. Linker, and R.S. Jones A polysaccharide resembling alginic acid from a pseudomonas micro-organism Nature 204 1964 187 188
29. C. Liu, C. Sun, H. Huang, K. Janda, and T. Edgington Overexpression of legumain in tumors is significant for invasion/metastasis and a candidate enzymatic target for prodrug therapy Cancer Research 63 11 2003 2957 2964 (Pubitemid 36667169)
30. B. Manoury, E.W. Hewitt, N. Morrice, P.M. Dando, A.J. Barrett, and C. Watts An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation Nature 396 6712 1998 695 699 (Pubitemid 29003950)
31. R.V. Murthy, G. Arbman, J. Gao, G.D. Roodman, and X.F. Sun Legumain expression in relation to clinicopathologic and biological variables in colorectal cancer Clinical Cancer Research 11 6 2005 2293 2299 (Pubitemid 40490189)
32. 2+ on alginate microbeads Biomacromolecules 7 5 2006 1471 1480 (Pubitemid 43811202)
33. M. Novak, and V. Vetvicka Glucans as biological response modifiers Endocrine, Metabolic & Immune Disorders - Drug Targets 9 1 2009 67 75
34. M. Otterlei, A. Sundan, G. Skjåk-Bræk, L. Ryan, O. Smidsrød, and T. Espevik Similar mechanisms of action of defined polysaccharides and lipopolysaccharides: characterization of binding and tumor necrosis factor alpha induction Infection and Immunity 61 5 1993 1917 1925 (Pubitemid 23145894)
35. M. Otterlei, K. Ostgaard, G. Skjåk-Bræk, O. Smidsrød, P. Soon-Shiong, and T. Espevik Induction of cytokine production from human monocytes stimulated with alginate Journal of Immunotherapy: Official Journal of the Society for Biological Therapy 10 4 1991 286 291
36. L.A. Price, C.A. Wenner, D.T. Sloper, J.W. Slaton, and J.P. Novack Role for toll-like receptor 4 in TNF-alpha secretion by murine macrophages in response to polysaccharide Krestin, a Trametes versicolor mushroom extract Fitoterapia 81 7 2010 914 919
37. I.A. Schepetkin, and M.T. Quinn Botanical polysaccharides: macrophage immunomodulation and therapeutic potential International Immunopharmacology 6 3 2006 317 333 (Pubitemid 43120446)
38. K. Shirahama-Noda, A. Yamamoto, K. Sugihara, N. Hashimoto, M. Asano, and M. Nishimura Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice The Journal of Biological Chemistry 278 35 2003 33194 33199 (Pubitemid 37055767)
39. R. Smith, H.T. Johansen, H. Nilsen, M.H. Haugen, S.J. Pettersen, and G.M. Maelandsmo Intra- and extracellular regulation of activity and processing of legumain by cystatin E/M Biochimie 94 12 2012 2590 2599
40. A. Thomas, K.G. Harding, and K. Moore Alginates from wound dressings activate human macrophages to secrete tumour necrosis factor-alpha Biomaterials 21 17 2000 1797 1802 (Pubitemid 30365043)
41. P. Vaupel, F. Kallinowski, and P. Okunieff Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review Cancer Research 49 23 1989 6449 6465 (Pubitemid 20008770)
42. K. Wolk, G. Grutz, K. Witte, H.D. Volk, and R. Sabat The expression of legumain, an asparaginyl endopeptidase that controls antigen processing, is reduced in endotoxin-tolerant monocytes Genes & Immunity 6 5 2005 452 456 (Pubitemid 43090523)
43. W. Wu, Y. Luo, C. Sun, Y. Liu, P. Kuo, and J. Varga Targeting cell-impermeable prodrug activation to tumor microenvironment eradicates multiple drug-resistant neoplasms Cancer Research 66 2 2006 970 980 (Pubitemid 43165965)
44. Y. Yamamoto, M. Kurachi, K. Yamaguchi, and T. Oda Induction of multiple cytokine secretion from RAW264.7 cells by alginate oligosaccharides Bioscience, Biotechnology, and Biochemistry 71 1 2007 238 241 (Pubitemid 46155170)