Granzyme B cleaves decorin, biglycan and soluble betaglycan, releasing active transforming growth factor-β1

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Boivin, Wendy A ^a,b   Shackleford, Marlo ^a   Vanden Hoek, Amanda ^b   Zhao, Hongyan ^a,b   Hackett, Tillie L ^a,b   Knight, Darryl A ^a,b   Granville, David J ^a,b  

^a ST PAUL S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DICHLOROISOCOUMARIN; BIGLYCAN; DECORIN; GRANZYME B; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; TRANSFORMING GROWTH FACTOR BETA1; 3,4-DICHLOROISOCOUMARIN; COUMARIN DERIVATIVE; GRANZYME; PROTEOGLYCAN; SERINE PROTEINASE INHIBITOR; SMAD3 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; CORONARY ARTERY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SMOOTH MUSCLE FIBER; TISSUE STRUCTURE; BIOCATALYSIS; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME SPECIFICITY; EXTRACELLULAR SPACE; KINETICS; METABOLISM; PHOSPHORYLATION; SOLUBILITY; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING;

BIGLYCAN; BIOCATALYSIS; BLOTTING, WESTERN; CELLS, CULTURED; COUMARINS; DECORIN; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; GRANZYMES; HUMANS; KINETICS; MUSCLE, SMOOTH, VASCULAR; PHOSPHORYLATION; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SERINE PROTEINASE INHIBITORS; SMAD3 PROTEIN; SOLUBILITY; SUBSTRATE SPECIFICITY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84859132892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033163     Document Type: Article

References (57)

1. Medema JP, Toes RE, Scaffidi C, Zheng TS, Flavell RA, et al. (1997) Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur J Immunol 27: 3492-3498.
2. Boivin WA, Cooper DM, Hiebert PR, Granville DJ, (2009) Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab Invest 89: 1195-1220.
3. Hendel A, Hiebert PR, Boivin WA, Williams SJ, Granville DJ, (2010) Granzymes in age-related cardiovascular and pulmonary diseases. Cell Death Differ 17: 596-606.
4. Bratke K, Bottcher B, Leeder K, Schmidt S, Kupper M, et al. (2004) Increase in granzyme B+ lymphocytes and soluble granzyme B in bronchoalveolar lavage of allergen challenged patients with atopic asthma. Clin Exp Immunol 136: 542-548.
5. Spaeny-Dekking EH, Hanna WL, Wolbink AM, Wever PC, Kummer AJ, et al. (1998) Extracellular granzymes A and B in humans: detection of native species during CTL responses in vitro and in vivo. J Immunol 160: 3610-3616.
6. Young LH, Joag SV, Lin PY, Luo SF, Zheng LM, et al. (1992) Expression of cytolytic mediators by synovial fluid lymphocytes in rheumatoid arthritis. Am J Pathol 140: 1261-1268.
7. Kondo H, Hojo Y, Tsuru R, Nishimura Y, Shimizu H, et al. (2009) Elevation of plasma granzyme B levels after acute myocardial infarction. Circ J 73: 503-507.
8. Chamberlain CM, Ang LS, Boivin WA, Cooper DM, Williams SJ, et al. (2010) Perforin-independent extracellular granzyme B activity contributes to abdominal aortic aneurysm. Am J Pathol 176: 1038-1049.
9. Ang LS, Boivin WA, Williams SJ, Zhao H, Abraham T, et al. (2011) Serpina3n attenuates granzyme B-mediated decorin cleavage and rupture in a murine model of aortic aneurysm. Cell Death Dis 2: e215.
10. Hiebert PR, Boivin WA, Abraham T, Pazooki S, Zhao H, et al. (2011) Granzyme B contributes to extracellular matrix remodeling and skin aging in apolipoprotein E knockout mice. Exp Gerontol 46: 489-499.
11. Gahring L, Carlson NG, Meyer EL, Rogers SW, (2001) Granzyme B proteolysis of a neuronal glutamate receptor generates an autoantigen and is modulated by glycosylation. J Immunol 166: 1433-1438.
12. Froelich CJ, Zhang X, Turbov J, Hudig D, Winkler U, et al. (1993) Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J Immunol 151: 7161-7171.
13. Buzza MS, Dyson JM, Choi H, Gardiner EE, Andrews RK, et al. (2008) Antihemostatic activity of human granzyme B mediated by cleavage of von Willebrand factor. J Biol Chem 283: 22498-22504.
14. Mulligan-Kehoe MJ, Drinane MC, Mollmark J, Casciola-Rosen L, Hummers LK, et al. (2007) Antiangiogenic plasma activity in patients with systemic sclerosis. Arthritis Rheum 56: 3448-3458.
15. Choy JC, Hung VH, Hunter AL, Cheung PK, Motyka B, et al. (2004) Granzyme B induces smooth muscle cell apoptosis in the absence of perforin: involvement of extracellular matrix degradation. Arterioscler Thromb Vasc Biol 24: 2245-2250.
16. Buzza MS, Zamurs L, Sun J, Bird CH, Smith AI, et al. (2005) Extracellular matrix remodeling by human granzyme B via cleavage of vitronectin, fibronectin, and laminin. J Biol Chem 280: 23549-23558.
17. Macri L, Silverstein D, Clark RA, (2007) Growth factor binding to the pericellular matrix and its importance in tissue engineering. Adv Drug Deliv Rev 59: 1366-1381.
18. Imai K, Hiramatsu A, Fukushima D, Pierschbacher MD, Okada Y, (1997) Degradation of decorin by matrix metalloproteinases: identification of the cleavage sites, kinetic analyses and transforming growth factor-beta1 release. Biochem J 322 (Pt 3): 809-814.
19. Taylor AW, (2009) Review of the activation of TGF-beta in immunity. J Leukoc Biol 85: 29-33.
20. Schiller M, Javelaud D, Mauviel A, (2004) TGF-beta-induced SMAD signaling and gene regulation: consequences for extracellular matrix remodeling and wound healing. J Dermatol Sci 35: 83-92.
21. Dallas SL, Miyazono K, Skerry TM, Mundy GR, Bonewald LF, (1995) Dual role for the latent transforming growth factor-beta binding protein in storage of latent TGF-beta in the extracellular matrix and as a structural matrix protein. J Cell Biol 131: 539-549.
22. Lopez-Casillas F, Payne HM, Andres JL, Massague J, (1994) Betaglycan can act as a dual modulator of TGF-beta access to signaling receptors: mapping of ligand binding and GAG attachment sites. J Cell Biol 124: 557-568.
23. Hildebrand A, Romaris M, Rasmussen LM, Heinegard D, Twardzik DR, et al. (1994) Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem J 302 (Pt 2): 527-534.
24. Fleischmajer R, Fisher LW, MacDonald ED, Jacobs L Jr, Perlish JS, et al. (1991) Decorin interacts with fibrillar collagen of embryonic and adult human skin. J Struct Biol 106: 82-90.
25. Schonherr E, Witsch-Prehm P, Harrach B, Robenek H, Rauterberg J, et al. (1995) Interaction of biglycan with type I collagen. J Biol Chem 270: 2776-2783.
26. Velasco-Loyden G, Arribas J, Lopez-Casillas F, (2004) The shedding of betaglycan is regulated by pervanadate and mediated by membrane type matrix metalloprotease-1. J Biol Chem 279: 7721-7733.
27. Arribas J, Borroto A, (2002) Protein ectodomain shedding. Chem Rev 102: 4627-4638.
28. Mythreye K, Blobe GC, (2009) Proteoglycan signaling co-receptors: roles in cell adhesion, migration and invasion. Cell Signal 21: 1548-1558.
29. Isaaz S, Baetz K, Olsen K, Podack E, Griffiths GM, (1995) Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway. Eur J Immunol 25: 1071-1079.
30. Prakash MD, Bird CH, Bird PI, (2009) Active and zymogen forms of granzyme B are constitutively released from cytotoxic lymphocytes in the absence of target cell engagement. Immunol Cell Biol 87: 249-254.
31. Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, et al. (2011) Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1alpha. Mol Cell 44: 265-278.
32. Tak PP, Spaeny-Dekking L, Kraan MC, Breedveld FC, Froelich CJ, et al. (1999) The levels of soluble granzyme A and B are elevated in plasma and synovial fluid of patients with rheumatoid arthritis (RA). Clin Exp Immunol 116: 366-370.
33. Raja SM, Wang B, Dantuluri M, Desai UR, Demeler B, et al. (2002) Cytotoxic cell granule-mediated apoptosis. Characterization of the macromolecular complex of granzyme B with serglycin. J Biol Chem 277: 49523-49530.
34. Raja SM, Metkar SS, Honing S, Wang B, Russin WA, et al. (2005) A novel mechanism for protein delivery: granzyme B undergoes electrostatic exchange from serglycin to target cells. J Biol Chem 280: 20752-20761.
35. Bird CH, Sun J, Ung K, Karambalis D, Whisstock JC, et al. (2005) Cationic sites on granzyme B contribute to cytotoxicity by promoting its uptake into target cells. Mol Cell Biol 25: 7854-7867.
36. Veugelers K, Motyka B, Goping IS, Shostak I, Sawchuk T, et al. (2006) Granule-mediated killing by granzyme B and perforin requires a mannose 6-phosphate receptor and is augmented by cell surface heparan sulfate. Mol Biol Cell 17: 623-633.
37. Ronday HK, van der Laan WH, Tak PP, de Roos JA, Bank RA, et al. (2001) Human granzyme B mediates cartilage proteoglycan degradation and is expressed at the invasive front of the synovium in rheumatoid arthritis. Rheumatology (Oxford) 40: 55-61.
38. Ito S, Taguchi H, Hamada S, Kawauchi S, Ito H, et al. (2008) Enzymatic properties of cellobiose 2-epimerase from Ruminococcus albus and the synthesis of rare oligosaccharides by the enzyme. Appl Microbiol Biotechnol 79: 433-441.
39. Kratzer R, Pukl M, Egger S, Vogl M, Brecker L, et al. (2011) Enzyme identification and development of a whole-cell biotransformation for asymmetric reduction of o-chloroacetophenone. Biotechnol Bioeng 108: 797-803.
40. Bae YA, Kim SH, Lee EG, Sohn WM, Kong Y, (2011) Identification and biochemical characterization of two novel peroxiredoxins in a liver fluke, Clonorchis sinensis. Parasitology 138: 1143-1153.
41. Chau Y, Tan FE, Langer R, (2004) Synthesis and characterization of dextran-peptide-methotrexate conjugates for tumor targeting via mediation by matrix metalloproteinase II and matrix metalloproteinase IX. Bioconjug Chem 15: 931-941.
42. Ling HB, Wang GJ, Li JE, Tan HR, (2008) sanN encoding a dehydrogenase is essential for Nikkomycin biosynthesis in Streptomyces ansochromogenes. J Microbiol Biotechnol 18: 397-403.
43. Casciola-Rosen L, Garcia-Calvo M, Bull HG, Becker JW, Hines T, et al. (2007) Mouse and human granzyme B have distinct tetrapeptide specificities and abilities to recruit the bid pathway. J Biol Chem 282: 4545-4552.
44. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, et al. (2006) The major human and mouse granzymes are structurally and functionally divergent. J Cell Biol 175: 619-630.
45. Harris JL, Peterson EP, Hudig D, Thornberry NA, Craik CS, (1998) Definition and redesign of the extended substrate specificity of granzyme B. J Biol Chem 273: 27364-27373.
46. Van Damme P, Maurer-Stroh S, Plasman K, Van Durme J, Colaert N, et al. (2009) Analysis of protein processing by N-terminal proteomics reveals novel species-specific substrate determinants of granzyme B orthologs. Mol Cell Proteomics 8: 258-272.
47. Tamarina NA, Grassi MA, Johnson DA, Pearce WH, (1998) Proteoglycan gene expression is decreased in abdominal aortic aneurysms. J Surg Res 74: 76-80.
48. Mohamed SA, Sievers HH, Hanke T, Richardt D, Schmidtke C, et al. (2009) Pathway analysis of differentially expressed genes in patients with acute aortic dissection. Biomark Insights 4: 81-90.
49. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, et al. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136: 729-743.
50. Gambichler T, Tomi NS, Skrygan M, Altmeyer P, Kreuter A, (2007) Significant decrease of decorin expression in human skin following short-term ultraviolet exposures. J Dermatol Sci 45: 203-205.
51. Mukhopadhyay A, Wong MY, Chan SY, Do DV, Khoo A, et al. (2010) Syndecan-2 and decorin: proteoglycans with a difference-implications in keloid pathogenesis. J Trauma 68: 999-1008.
52. Carrino DA, Mesiano S, Barker NM, Hurd WW, Caplan AI, (2012) Proteoglycans of uterine fibroids and keloid scars: similarity in their proteoglycan composition. Biochem J.
53. Wu J, Utani A, Endo H, Shinkai H, (2001) Deficiency of the decorin core protein in the variant form of Ehlers-Danlos syndrome with chronic skin ulcer. J Dermatol Sci 27: 95-103.
54. Amalinei C, Caruntu ID, Balan RA, (2007) Biology of metalloproteinases. Rom J Morphol Embryol 48: 323-334.
55. Chang C, Werb Z, (2001) The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 11: S37-43.
56. Thomas DA, Massague J, (2005) TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8: 369-380.
57. Granville DJ, (2010) Granzymes in disease: bench to bedside. Cell Death Differ 17: 565-566.