Granzyme B cleavage of fibronectin disrupts endothelial cell adhesion, migration and capillary tube formation

Matrix Biology

Volumn 32, Issue 1, 2013, Pages 14-22

  Hendel, Alon ^a,b   Granville, David J ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ST PAUL S HOSPITAL   (Canada)

Author keywords

Angiogenesis; Endothelial cell; Extracellular matrix; Fibronectin; Granzyme B

Indexed keywords

FIBRONECTIN; GRANZYME B;

ANGIOGENESIS; ARTICLE; CAPILLARY TUBE; CELL ADHESION; CELL MIGRATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SECRETION;

ANALYSIS OF VARIANCE; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FIBRONECTINS; GRANZYMES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84873258027     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2012.11.013     Document Type: Article

References (62)

1. Abraham T., Carthy J., McManus B. Collagen matrix remodeling in 3-dimensional cellular space resolved using second harmonic generation and multiphoton excitation fluorescence. J. Struct. Biol. 2010, 169:36-44.
2. Ambesi A., Klein R.M., Pumiglia K.M., McKeown-Longo P.J. Anastellin, a fragment of the first type III repeat of fibronectin, inhibits extracellular signal-regulated kinase and causes G(1) arrest in human microvessel endothelial cells. Cancer Res. 2005, 65:148-156.
3. Arroyo A.G., Iruela-Arispe M.L. Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc. Res. 2010, 86(2):226-235.
4. Astrof S., Hynes R.O. Fibronectins in vascular morphogenesis. Angiogenesis 2009, 12:165-175.
5. Barilla M.L., Carsons S.E. Fibronectin fragments and their role in inflammatory arthritis. Semin. Arthritis Rheum. 2000, 29:252-265.
6. Boivin W.A., Cooper D.M., Hiebert P.R., Granville D.J. Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab. Invest. 2009, 89:1195-1220.
7. Buzza M.S., Bird P.I. Extracellular granzymes: current perspectives. Biol. Chem. 2006, 387:827-837.
8. Buzza M.S., Zamurs L., Sun J., Bird C.H., Smith A.I., Trapani J.A., Froelich C.J., Nice E.C., Bird P.I. Extracellular matrix remodeling by human granzyme B via cleavage of vitronectin, fibronectin, and laminin. J. Biol. Chem. 2005, 280:23549-23558.
9. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 2000, 6:389-395.
10. Carmeliet P. Angiogenesis in health and disease. Nat. Med. 2003, 9:653-660.
11. Chamberlain C.M., Ang L.S., Boivin W.A., Cooper D.M., Williams S.J., Zhao H., Hendel A., Folkesson M., Swedenborg J., Allard M.F., McManus B.M., Granville D.J. Perforin-independent extracellular granzyme B activity contributes to abdominal aortic aneurysm. Am. J. Pathol. 2010, 176:1038-1049.
12. Choy J.C., Hung V.H., Hunter A.L., Cheung P.K., Motyka B., Goping I.S., Sawchuk T., Bleackley R.C., Podor T.J., McManus B.M., Granville D.J. Granzyme B induces smooth muscle cell apoptosis in the absence of perforin: involvement of extracellular matrix degradation. Arterioscler. Thromb. Vasc. Biol. 2004, 24:2245-2250.
13. Choy J.C., Kerjner A., Wong B.W., McManus B.M., Granville D.J. Perforin mediates endothelial cell death and resultant transplant vascular disease in cardiac allografts. Am. J. Pathol. 2004, 165:127-133.
14. Choy J.C., Cruz R.P., Kerjner A., Geisbrecht J., Sawchuk T., Fraser S.A., Hudig D., Bleackley R.C., Jirik F.R., McManus B.M., Granville D.J. Granzyme B induces endothelial cell apoptosis and contributes to the development of transplant vascular disease. Am. J. Transplant. 2005, 5:494-499.
15. Costa C., Incio J., Soares R. Angiogenesis and chronic inflammation: cause or consequence?. Angiogenesis 2007, 10:149-166.
16. Davis G.E. Angiogenesis and proteinases: influence on vascular morphogenesis, stabilization and regression. Drug Discov. Today Dis. Models 2011, 8:13-20.
17. Davis G.E., Senger D.R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 2005, 97:1093-1107.
18. Davis G.E., Bayless K.J., Davis M.J., Meininger G.A. Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am. J. Pathol. 2000, 156:1489-1498.
19. Davis G.E., Bayless K.J., Mavila A. Molecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat. Rec. 2002, 268:252-275.
20. D'Eliseo D., Pisu P., Romano C., Tubaro A., De Nunzio C., Morrone S., Santoni A., Stoppacciaro A., Velotti F. Granzyme B is expressed in urothelial carcinoma and promotes cancer cell invasion. Int. J. Cancer 2009, 127:1283-1294.
21. Froelich C.J., Zhang X., Turbov J., Hudig D., Winkler U., Hanna W.L. Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J. Immunol. 1993, 151:7161-7171.
22. Froelich C.J., Pardo J., Simon M.M. Granule-associated serine proteases: granzymes might not just be killer proteases. Trends Immunol. 2009, 30(3):117-123.
23. Fukai F., Ohtaki M., Fujii N., Yajima H., Ishii T., Nishizawa Y., Miyazaki K., Katayama T. Release of biological activities from quiescent fibronectin by a conformational change and limited proteolysis by matrix metalloproteinases. Biochemistry 1995, 34:11453-11459.
24. Glukhova M.A., Frid M.G., Shekhonin B.V., Vasilevskaya T.D., Grunwald J., Saginati M., Koteliansky V.E. Expression of extra domain A fibronectin sequence in vascular smooth muscle cells is phenotype dependent. J. Cell Biol. 1989, 109:357-366.
25. Grant M.B., Caballero S., Bush D.M., Spoerri P.E. Fibronectin fragments modulate human retinal capillary cell proliferation and migration. Diabetes 1998, 47:1335-1340.
26. Hendel A., Hiebert P.R., Boivin W.A., Williams S.J., Granville D.J. Granzymes in age-related cardiovascular and pulmonary diseases. Cell Death Differ. 2010, 17:596-606.
27. Hernandez-Pigeon H., Jean C., Charruyer A., Haure M.J., Titeux M., Tonasso L., Quillet-Mary A., Baudouin C., Charveron M., Laurent G. Human keratinocytes acquire cellular cytotoxicity under UV-B irradiation. Implication of granzyme B and perforin. J. Biol. Chem. 2006, 281:13525-13532.
28. Hernandez-Pigeon H., Jean C., Charruyer A., Haure M.J., Baudouin C., Charveron M., Quillet-Mary A., Laurent G. UVA induces granzyme B in human keratinocytes through MIF: implication in extracellular matrix remodeling. J. Biol. Chem. 2007, 282:8157-8164.
29. Homandberg G.A., Williams J.E., Grant D., Schumacher B., Eisenstein R. Heparin-binding fragments of fibronectin are potent inhibitors of endothelial cell growth. Am. J. Pathol. 1985, 120:327-332.
30. Humphries M.J., Obara M., Olden K., Yamada K.M. Role of fibronectin in adhesion, migration, and metastasis. Cancer Invest. 1989, 7:373-393.
31. Hynes R.O. Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 2007, 5(Suppl. 1):32-40.
32. Isaaz S., Baetz K., Olsen K., Podack E., Griffiths G.M. 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. 1995, 25:1071-1079.
33. Jackson J.R., Seed M.P., Kircher C.H., Willoughby D.A., Winkler J.D. The codependence of angiogenesis and chronic inflammation. FASEB J. 1997, 11:457-465.
34. Katayama M., Kamihagi K., Nakagawa K., Akiyama T., Sano Y., Ouchi R., Nagata S., Hino F., Kato I. Increased fragmentation of urinary fibronectin in cancer patients detected by immunoenzymometric assay using domain-specific monoclonal antibodies. Clin. Chim. Acta 1993, 217:115-128.
35. Labat-Robert J. Age-dependent remodeling of connective tissue: role of fibronectin and laminin. Pathol. Biol. (Paris) 2003, 51:563-568.
36. Mosher D.F. Fibronectin 1989, Academic Press, Inc., San Diego.
37. Owens R.J., Kornblihtt A.R., Baralle F.E. Fibronectin, the generation of multiple polypeptides from a single gene. Oxf. Surv. Eukaryot. Genes 1986, 3:141-160.
38. Pagano M., Reboud-Ravaux M. Cryptic activities of fibronectin fragments, particularly cryptic proteases. Front. Biosci. 2011, 16:698-706.
39. Pankov R., Yamada K.M. Fibronectin at a glance. J. Cell Sci. 2002, 115:3861-3863.
40. Pardo J., Wallich R., Ebnet K., Iden S., Zentgraf H., Martin P., Ekiciler A., Prins A., Mullbacher A., Huber M., Simon M.M. Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin. Cell Death Differ. 2007, 14:1768-1779.
41. Paul J.I., Schwarzbauer J.E., Tamkun J.W., Hynes R.O. Cell-type-specific fibronectin subunits generated by alternative splicing. J. Biol. Chem. 1986, 261:12258-12265.
42. Prakash M.D., Bird C.H., Bird P.I. Active and zymogen forms of granzyme B are constitutively released from cytotoxic lymphocytes in the absence of target cell engagement. Immunol. Cell Biol. 2009, 87:249-254.
43. Ronday H.K., van der Laan W.H., Tak P.P., de Roos J.A., Bank R.A., TeKoppele J.M., Froelich C.J., Hack C.E., Hogendoorn P.C., Breedveld F.C., Verheijen J.H. Human granzyme B mediates cartilage proteoglycan degradation and is expressed at the invasive front of the synovium in rheumatoid arthritis. Rheumatology (Oxford) 2001, 40:55-61.
44. Ruoslahti E., Pierschbacher M.D. New perspectives in cell adhesion: RGD and integrins. Science 1987, 238:491-497.
45. Saito S., Murakoshi K., Kotake S., Kamatani N., Tomatsu T. Granzyme B induces apoptosis of chondrocytes with natural killer cell-like cytotoxicity in rheumatoid arthritis. J. Rheumatol. 2008, 35:1932-1943.
46. Schechner J.S., Nath A.K., Zheng L., Kluger M.S., Hughes C.C., Sierra-Honigmann M.R., Lorber M.I., Tellides G., Kashgarian M., Bothwell A.L., Pober J.S. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:9191-9196.
47. Schwarzbauer J.E., DeSimone D.W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 2011, 3.
48. Senger D.R., Perruzzi C.A., Streit M., Koteliansky V.E., de Fougerolles A.R., Detmar M. The alpha(1)beta(1) and alpha(2)beta(1) integrins provide critical support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor angiogenesis. Am. J. Pathol. 2002, 160:195-204.
49. Silva R., D'Amico G., Hodivala-Dilke K.M., Reynolds L.E. Integrins: the keys to unlocking angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2008, 28:1703-1713.
50. Sottile J. Regulation of angiogenesis by extracellular matrix. Biochim. Biophys. Acta 2004, 1654:13-22.
51. Stanley C.M., Wang Y., Pal S., Klebe R.J., Harkless L.B., Xu X., Chen Z., Steffensen B. Fibronectin fragmentation is a feature of periodontal disease sites and diabetic foot and leg wounds and modifies cell behavior. J. Periodontol. 2008, 79:861-875.
52. Szekanecz Z., Koch A.E. Mechanisms of disease: angiogenesis in inflammatory diseases. Nat. Clin. Pract. Rheumatol. 2007, 3:635-643.
53. van Hinsbergh V.W., Engelse M.A., Quax P.H. Pericellular proteases in angiogenesis and vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 2006, 26:716-728.
54. Vartio T., Seppa H., Vaheri A. Susceptibility of soluble and matrix fibronectins to degradation by tissue proteinases, mast cell chymase and cathepsin G. J. Biol. Chem. 1981, 256:471-477.
55. Vartio T., Laitinen L., Narvanen O., Cutolo M., Thornell L.E., Zardi L., Virtanen I. Differential expression of the ED sequence-containing form of cellular fibronectin in embryonic and adult human tissues. J. Cell Sci. 1987, 88(Pt 4):419-430.
56. Verneuil L., Leboeuf C., Vidal J.S., Ratajczak P., Comoz F., Ameisen J.C., Janin A. Endothelial damage in all types of T-lymphocyte-mediated drug-induced eruptions. Arch. Dermatol. 2011, 147:579-584.
57. Waterhouse N.J., Sedelies K.A., Clarke C.J. Granzyme B; the chalk-mark of a cytotoxic lymphocyte. J. Transl. Med. 2004, 2:36.
58. Wayner E.A., Carter W.G., Piotrowicz R.S., Kunicki T.J. The function of multiple extracellular matrix receptors in mediating cell adhesion to extracellular matrix: preparation of monoclonal antibodies to the fibronectin receptor that specifically inhibit cell adhesion to fibronectin and react with platelet glycoproteins Ic-IIa. J. Cell Biol. 1988, 107:1881-1891.
59. Willoughby C.A., Bull H.G., Garcia-Calvo M., Jiang J., Chapman K.T., Thornberry N.A. Discovery of potent, selective human granzyme B inhibitors that inhibit CTL mediated apoptosis. Bioorg. Med. Chem. Lett. 2002, 12:2197-2200.
60. Wilson S.H., Ljubimov A.V., Morla A.O., Caballero S., Shaw L.C., Spoerri P.E., Tarnuzzer R.W., Grant M.B. Fibronectin fragments promote human retinal endothelial cell adhesion and proliferation and ERK activation through alpha5beta1 integrin and PI 3-kinase. Invest. Ophthalmol. Vis. Sci. 2003, 44:1704-1715.
61. Yamada K.M. Fibronectin peptides in cell migration and wound repair. J. Clin. Invest. 2000, 105:1507-1509.
62. Zhou X., Rowe R.G., Hiraoka N., George J.P., Wirtz D., Mosher D.F., Virtanen I., Chernousov M.A., Weiss S.J. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 2008, 22:1231-1243.