The TLR4 agonist fibronectin extra domain a is cryptic, Exposed by elastase-2; Use in a fibrin matrix cancer vaccine

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Julier, Ziad ^a   Martino, Mikaël M ^a,b   De Titta, Alexandre ^a   Jeanbart, Laura ^a   Hubbell, Jeffrey A ^a,c,d  

^a EPFL   (Switzerland)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF CHICAGO   (United States)

^d ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; FIBRIN; FIBRONECTIN; LIPOPOLYSACCHARIDE; OVALBUMIN; PANCREATIC ELASTASE II; RECOMBINANT PROTEIN; SERINE PROTEINASE; TOLL LIKE RECEPTOR 4;

AGONISTS; ALLOTRANSPLANTATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CD8+ T LYMPHOCYTE; CHEMISTRY; CYTOLOGY; DISEASE MODEL; GENETICS; IMMUNOLOGY; MELANOMA, EXPERIMENTAL; METABOLISM; MOUSE; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FIBRIN; FIBRONECTINS; LIPOPOLYSACCHARIDES; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; OVALBUMIN; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; TOLL-LIKE RECEPTOR 4; TRANSPLANTATION, HOMOLOGOUS;

EID: 84923878415     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08569     Document Type: Article

References (58)

1. Pankov, R. & Yamada, K. M. Fibronectin at a glance. J. Cell Sci. 115, 3861-3863 (2002).
2. Ffrench-Constant, C. Alternative splicing of fibronectin-many different proteins but few different functions. Exp. Cell Res. 221, 261-71 (1995).
3. Ffrench-Constant, C. & Hynes, R. O. Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo. Development 106, 375-88 (1989).
4. Jarnagin, W. R., Rockey, D. C., Koteliansky, V. E., Wang, S. S. & Bissell, D. M. Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J. Cell Biol. 127, 2037-48 (1994).
5. Liao, Y. F., Gotwals, P. J., Koteliansky, V. E., Sheppard, D.& Van De Water, L. The EIIIA segment of fibronectin is a ligand for integrins alpha 9beta 1 and alpha 4beta 1 providing a novel mechanism for regulating cell adhesion by alternative splicing. J. Biol. Chem. 277, 14467-74 (2002).
6. Ffrench-Constant, C., Van de Water, L., Dvorak, H. F. & Hynes, R. O. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat. J. Cell Biol. 109, 903-14 (1989).
7. Rybak, J. N., Roesli, C., Kaspar, M., Villa, A. & Neri, D. The extra-domain A of fibronectin is a vascular marker of solid tumors and metastases. Cancer Res. 67, 10948-57 (2007).
8. Villa, A. et al. A high-affinity human monoclonal antibody specific to the alternatively spliced EDA domain of fibronectin efficiently targets tumor neovasculature in vivo. Int. J. Cancer 122, 2405-13 (2008).
9. Borsi, L., Castellani, P., Allemanni, G., Neri, D. & Zardi, L. Preparation of phage antibodies to the ED-A domain of human fibronectin. Exp. Cell Res. 240, 244-51 (1998).
10. McFadden, J. P., Baker, B. S., Powles, A. V. & Fry, L. Psoriasis and extra domain A fibronectin loops. Br. J. Dermatol. 163, 5-11 (2010).
11. McFadden, J. P., Baker, B. S., Powles, A. V. & Fry, L. Psoriasis and streptococci: postscript regarding extra domain A fibronectin. Br. J. Dermatol. 161, 706-7 (2009).
12. McFadden, J., Fry, L., Powles, A. V. & Kimber, I. Concepts in psoriasis: psoriasis and the extracellular matrix. Br. J. Dermatol. 167, 980-6 (2012).
13. Astrof, S., Crowley, D. & Hynes, R. O. Multiple cardiovascular defects caused by the absence of alternatively spliced segments of fibronectin. Dev. Biol. 311, 11-24 (2007).
14. Okamura, Y. et al. The extra domain Aof fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276, 10229-33 (2001).
15. Bhattacharyya, S. et al. FibronectinEDA promotes chronic cutaneous fibrosis through Toll-like receptor signaling. Sci. Transl. Med. 6, 232ra50 (2014).
16. Charo, I. F., Nannizzi, L., Smith, J.W. & Cheresh, D. A. The vitronectin receptor alpha v beta 3 binds fibronectin and acts in concert with alpha 5 beta 1 in promoting cellular attachment and spreading on fibronectin. J. Cell Biol. 111, 2795-800 (1990).
17. Redick, S. D., Settles, D. L., Briscoe, G. Erickson,H. P.Defining fibronectin's cell adhesion synergy site by site-directed mutagenesis. J. Cell Biol. 149, 521-7 (2000).
18. Ohashi, T. & Erickson, H. P. Domain unfolding plays a role in superfibronectin formation. J. Biol. Chem. 280, 39143-51 (2005).
19. Mostafavi-Pour, Z., Askari, J. A.,Whittard, J. D.Humphries, M. J. Identification of a novel heparin-binding site in the alternatively spliced IIICS region of fibronectin: roles of integrins and proteoglycans in cell adhesion to fibronectin splice variants. Matrix Biol. 20, 63-73 (2001).
20. Martino, M. M. & Hubbell, J. A. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 24, 4711-21 (2010).
21. Wijelath, E. S. et al. Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain: enhancement of VEGF biological activity by a singular growth factor/matrix protein synergism. Circ. Res. 99, 853-60 (2006).
22. Martino, M. M. et al. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 3, 100ra89 (2011).
23. Lin, F. et al. Fibronectin growth factor-binding domains are required for fibroblast survival. J. Invest. Dermatol. 131, 84-98 (2011).
24. Saito, S. et al. The fibronectin extra domain A activates matrix metalloproteinase gene expression by an interleukin-1-dependent mechanism. J. Biol. Chem. 274, 30756-63 (1999).
25. Sekiguchi, K. & Hakomori, S. Functional domain structure of fibronectin. Proc. Natl. Acad. Sci. U. S. A. 77, 2661-5 (1980).
26. Arribillaga, L. et al. A fusion protein between streptavidin and the endogenous TLR4 ligand EDA targets biotinylated antigens to dendritic cells and induces T cell responses in vivo. Biomed Res. Int. 2013, 864720 (2013).
27. Mansilla, C. et al. Immunization against hepatitis C virus with a fusion protein containing the extra domain A from fibronectin and the hepatitis C virus NS3 protein. J. Hepatol. 51, 520-7 (2009).
28. Mansilla, C. et al. Eradication of large tumors expressing human papillomavirus E7 protein by therapeutic vaccination with E7 fused to the extra domain a from fibronectin. Int. J. Cancer 131, 641-51 (2012).
29. San Román, B. et al. The extradomain A of fibronectin (EDA) combined with poly(I:C) enhances the immune response to HIV-1 p24 protein and the protection against recombinant Listeria monocytogenes-Gag infection in the mouse model. Vaccine 30, 2564-9 (2012).
30. Lasarte, J. J. et al. The extra domain A from fibronectin targets antigens to TLR4-expressing cells and induces cytotoxic T cell responses in vivo. J. Immunol. 178, 748-56 (2007).
31. Rudilla, F. et al. Combination of a TLR4 ligand and anaphylatoxin C5a for the induction of antigen-specific cytotoxic T cell responses. Vaccine 30, 2848-58 (2012).
32. Song, J. et al. PROSPER: an integrated feature-based tool for predicting protease substrate cleavage sites. PLoS One 7, e50300 (2012).
33. Lipford, G. B., Bauer, S., Wagner, H.Heeg, K. In vivo CTL induction with pointsubstituted ovalbumin peptides: immunogenicity correlates with peptide-induced MHC class I stability. Vaccine 13, 313-20 (1995).
34. Ali, O. A., Emerich, D., Dranoff, G. & Mooney, D. J. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci. Transl. Med. 1, 8ra19 (2009).
35. Schense, J. C. & Hubbell, J. A. Cross-linking exogenous bifunctional peptides into fibrin gels with factor XIIIa. Bioconjug. Chem. 10, 75-81 (1999).
36. Craiu, A., Akopian, T., Goldberg, A. & Rock, K. L. Two distinct proteolytic processes in the generation of a major histocompatibility complex class Ipresented peptide. Proc. Natl. Acad. Sci. U. S. A. 94, 10850-5 (1997).
37. Martino, M. M. et al. Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability. Biomaterials 30, 1089-97 (2009).
38. Parkhurst, M. R. et al. Identification of a shared HLA-A∗0201-restricted T-cell epitope from the melanoma antigen tyrosinase-related protein 2 (TRP2). Cancer Res. 58, 4895-901 (1998).
39. Gabrilovich, D. I. & Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-74 (2009).
40. Dolcetti, L. et al. Myeloid-derived suppressor cell role in tumor-related inflammation. Cancer Lett. 267, 216-25 (2008).
41. George, E. L.,Georges-Labouesse, E. N., Patel-King, R. S., Rayburn, H.Hynes, R. O. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-91 (1993).
42. Valenick, L. V., Hsia, H. C. & Schwarzbauer, J. E. Fibronectin fragmentation promotes alpha4beta1 integrin-mediated contraction of a fibrin-fibronectin provisional matrix. Exp. Cell Res. 309, 48-55 (2005).
43. Plow, E. F., Haas, T. A., Zhang, L., Loftus, J. & Smith, J. W. Ligand binding to integrins. J. Biol. Chem. 275, 21785-8 (2000).
44. Zhong, C. et al. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539-51 (1998).
45. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7, 265-75 (2006).
46. 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. 156, 1489-98 (2000).
47. Shinde, A. V. et al. Identification of the peptide sequences within the EIIIA (EDA) segment of fibronectin that mediate integrin alpha9beta1-dependent cellular activities. J. Biol. Chem. 283, 2858-70 (2008).
48. Xaus, J. et al. LPS induces apoptosis in macrophages mostly through the autocrine production of TNF-alpha. Blood 95, 3823-31 (2000).
49. Baldwin, G. et al. Effect of polymyxin B on experimental shock from meningococcal and Escherichia coli endotoxins. J. Infect. Dis. 164, 542-9 (1991).
50. Karplus, T. E., Ulevitch, R. J. & Wilson, C. B. A new method for reduction of endotoxin contamination from protein solutions. J. Immunol. Methods 105, 211-20 (1987).
51. Toichi, E., Tachibana, T. & Furukawa, F. Rapid improvement of psoriasis vulgaris during drug-induced agranulocytosis. J. Am. Acad. Dermatol. 43, 391-5 (2000).
52. Wetzel, A. et al. Increased neutrophil adherence in psoriasis: role of the human endothelial cell receptor Thy-1 (CD90). J. Invest. Dermatol. 126, 441-52 (2006).
53. Schense, J. C., Bloch, J., Aebischer, P. & Hubbell, J. A. Enzymatic incorporation of bioactive peptides into fibrin matrices enhances neurite extension. Nat. Biotechnol. 18, 415-9 (2000).
54. Beaudette, T. T. et al. In vivo studies on the effect of co-encapsulation of CpG DNA and antigen in acid-degradable microparticle vaccines. Mol. Pharm. 6, 1160-9 (2010).
55. Breckpot, K. et al. Lentivirally transduced dendritic cells as a tool for cancer immunotherapy. J. Gene Med. 5, 654-67 (2003).
56. Jeanbart, L. et al. Enhancing efficacy of anticancer vaccines by targeted delivery to tumor-draining lymph nodes. Cancer Immunol. Res. 2, 436-47 (2014).
57. Lindau, D., Gielen, P., Kroesen, M., Wesseling, P. & Adema, G. J. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology 138, 105-15 (2013).
58. Lutz, M. B. et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92 (1999).