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Published in: Inflammation 2/2013

01-04-2013

An Extragranular Compartment of Blood Eosinophils Contains Eosinophil Protein X/Eosinophil-Derived Neurotoxin (EPX/EDN)

Authors: Malgorzata Karawajczyk, Christer G. B. Peterson, Per Venge, Rodolfo C. Garcia

Published in: Inflammation | Issue 2/2013

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Abstract

Serum and plasma profiles of eosinophil protein X (EPX/EDN) and those of other eosinophil proteins differ in various conditions, suggesting a different mobilisation from storage granules. This work studied the subcellular localisation of EPX/EDN in non-primed and in vivo primed blood eosinophils from healthy and allergic subjects, during and out of the pollen season. Primed eosinophils contain easily mobilisable secretory proteins. By fractionation on sucrose density gradients, EPX/EDN localised in the specific granules as well as in a cytoplasmic extra-granular compartment of low equilibrium density that partially overlapped with vesicular structures, cytosolic proteins and plasma membranes. This compartment was clearly separate from the low density peak of ECP that increases during the pollen season. There were no significant differences in the amounts of EPX/EDN present in the low density peak of healthy and allergic subjects. Immuno-gold labelling electron microscopy showed EPX/EDN in specific granules, cytoplasm and associated to plasma membranes. In conclusion, substantial amounts of EPX/EDN localise in an extra-granular, low equilibrium density compartment of human eosinophils.
Literature
1.
2.
go back to reference Adamko, D.J., S.O. Odemuyiwa, D. Vethanayagam, and R. Moqbel. 2005. The rise of the phoenix: the expanding role of the eosinophil in health and disease. Allergy 60: 13–22.PubMedCrossRef Adamko, D.J., S.O. Odemuyiwa, D. Vethanayagam, and R. Moqbel. 2005. The rise of the phoenix: the expanding role of the eosinophil in health and disease. Allergy 60: 13–22.PubMedCrossRef
3.
go back to reference Hogan, S.P., H.F. Rosenberg, R. Moqbel, S. Phipps, P.S. Foster, P. Lacy, A.B. Kay, and M.E. Rothenberg. 2008. Eosinophils: biological properties and role in health and disease. Clinical and Experimental Allergy 38: 709–750.PubMedCrossRef Hogan, S.P., H.F. Rosenberg, R. Moqbel, S. Phipps, P.S. Foster, P. Lacy, A.B. Kay, and M.E. Rothenberg. 2008. Eosinophils: biological properties and role in health and disease. Clinical and Experimental Allergy 38: 709–750.PubMedCrossRef
4.
go back to reference Peterson, C.G.B., and P. Venge. 1983. Purification and characterization of a new cationic protein - eosinophil protein X (EPX) - from granules of human eosinophils. Immunology 50: 19–26.PubMed Peterson, C.G.B., and P. Venge. 1983. Purification and characterization of a new cationic protein - eosinophil protein X (EPX) - from granules of human eosinophils. Immunology 50: 19–26.PubMed
5.
go back to reference Slifman, N.R., P. Venge, C.G. Peterson, D.J. McKean, and G.J. Gleich. 1989. Human eosinophil-derived neurotoxin and eosinophil protein X are likely the same protein. Journal of Immunology 143: 2317–2322. Slifman, N.R., P. Venge, C.G. Peterson, D.J. McKean, and G.J. Gleich. 1989. Human eosinophil-derived neurotoxin and eosinophil protein X are likely the same protein. Journal of Immunology 143: 2317–2322.
6.
go back to reference Gullberg, U., B. Widegren, U. Arnason, A. Egesten, and I. Olsson. 1986. The cytotoxic eosinophil cationic protein (ECP) has ribunoclease activity. Biochemical and Biophysical Research Communications 139: 1239–1242.PubMedCrossRef Gullberg, U., B. Widegren, U. Arnason, A. Egesten, and I. Olsson. 1986. The cytotoxic eosinophil cationic protein (ECP) has ribunoclease activity. Biochemical and Biophysical Research Communications 139: 1239–1242.PubMedCrossRef
7.
go back to reference Hamann, K.J., R.L. Barker, D.A. Loegering, L.R. Pease, and G.J. Gleich. 1989. Sequence of human eosinophil-derived neurotoxin cDNA: Identity of deduced amino acid sequence with human nonsecretory ribonucleases. Gene 83: 161–167.PubMedCrossRef Hamann, K.J., R.L. Barker, D.A. Loegering, L.R. Pease, and G.J. Gleich. 1989. Sequence of human eosinophil-derived neurotoxin cDNA: Identity of deduced amino acid sequence with human nonsecretory ribonucleases. Gene 83: 161–167.PubMedCrossRef
8.
go back to reference Durack, D.T., S.J. Ackerman, D.A. Loegering, and G.J. Gleich. 1981. Purification of human eosinophil-derived neurotoxin. Proceedings of the National Academy of Sciences USA 78: 5165–5169.CrossRef Durack, D.T., S.J. Ackerman, D.A. Loegering, and G.J. Gleich. 1981. Purification of human eosinophil-derived neurotoxin. Proceedings of the National Academy of Sciences USA 78: 5165–5169.CrossRef
9.
go back to reference Rosenberg, H.F., and J.B. Domachowske. 2001. Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. Journal of Leukocyte Biology 70: 691–698.PubMed Rosenberg, H.F., and J.B. Domachowske. 2001. Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. Journal of Leukocyte Biology 70: 691–698.PubMed
10.
go back to reference Yang, D., H.F. Rosenberg, Q. Chen, K.D. Dyer, K. Kurosaka, and J.J. Oppenheim. 2003. Eosinophil-derived neurotoxin (EDN), an antimicrobial protein with chemotactic activities for dendritic cells. Blood 102: 3396–3403.PubMedCrossRef Yang, D., H.F. Rosenberg, Q. Chen, K.D. Dyer, K. Kurosaka, and J.J. Oppenheim. 2003. Eosinophil-derived neurotoxin (EDN), an antimicrobial protein with chemotactic activities for dendritic cells. Blood 102: 3396–3403.PubMedCrossRef
11.
go back to reference Yang, D., Q. Chen, H.F. Rosenberg, S.M. Rybak, D.L. Newton, Z.Y. Wang, Q. Fu, V.T. Tchernev, M. Wang, B. Schweitzer, S.F. Kingsmore, D.D. Patel, J.J. Oppenheim, and O.M. Howard. 2004. Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. Journal of Immunology 173: 6134–6142. Yang, D., Q. Chen, H.F. Rosenberg, S.M. Rybak, D.L. Newton, Z.Y. Wang, Q. Fu, V.T. Tchernev, M. Wang, B. Schweitzer, S.F. Kingsmore, D.D. Patel, J.J. Oppenheim, and O.M. Howard. 2004. Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. Journal of Immunology 173: 6134–6142.
12.
go back to reference Yang, D., Q. Chen, S.B. Su, P. Zhang, K. Kurosaka, R.R. Caspi, S.M. Michalek, H.F. Rosenberg, N. Zhang, and J.J. Oppenheim. 2008. Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. The Journal of Experimental Medicine 205: 79–90.PubMedCrossRef Yang, D., Q. Chen, S.B. Su, P. Zhang, K. Kurosaka, R.R. Caspi, S.M. Michalek, H.F. Rosenberg, N. Zhang, and J.J. Oppenheim. 2008. Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. The Journal of Experimental Medicine 205: 79–90.PubMedCrossRef
13.
go back to reference Rosenberg, H.F., S.J. Ackerman, and D.G. Tenen. 1989. Human eosinophil cationic protein. Molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. Journal of Experimental Medicine 170: 163–176.PubMedCrossRef Rosenberg, H.F., S.J. Ackerman, and D.G. Tenen. 1989. Human eosinophil cationic protein. Molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. Journal of Experimental Medicine 170: 163–176.PubMedCrossRef
14.
go back to reference Peters, M.S., M. Rodriguez, and G.J. Gleich. 1986. Localization of human eosinophil granule major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin by immunoelectron microscopy. Laboratory Investigation 54: 656–662.PubMed Peters, M.S., M. Rodriguez, and G.J. Gleich. 1986. Localization of human eosinophil granule major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin by immunoelectron microscopy. Laboratory Investigation 54: 656–662.PubMed
15.
go back to reference Peterson, C.G.B., R.C. Garcia, M.G.Ch. Carlson, and P. Venge. 1987. Eosinophil cationic protein (ECP), eosinophil protein x (EPX) and eosinophil peroxidase (EPO): Granule distribution, degranulation and characterization of released proteins. In: Peterson, C.G.B. (Ed.), Eosinophil granule proteins: Biochemical and functional studies. Doctoral Thesis, Uppsala University, Uppsala, pp. 1–19. Peterson, C.G.B., R.C. Garcia, M.G.Ch. Carlson, and P. Venge. 1987. Eosinophil cationic protein (ECP), eosinophil protein x (EPX) and eosinophil peroxidase (EPO): Granule distribution, degranulation and characterization of released proteins. In: Peterson, C.G.B. (Ed.), Eosinophil granule proteins: Biochemical and functional studies. Doctoral Thesis, Uppsala University, Uppsala, pp. 1–19.
16.
go back to reference Venge, P., R. Dahl, and C.G.B. Peterson. 1988. Eosinophil granule proteins in serum after allergen challenge of asthmatic patients and the effects of anti-asthmatic medication. International Archives of Allergy and Immunology 87: 306–312.CrossRef Venge, P., R. Dahl, and C.G.B. Peterson. 1988. Eosinophil granule proteins in serum after allergen challenge of asthmatic patients and the effects of anti-asthmatic medication. International Archives of Allergy and Immunology 87: 306–312.CrossRef
17.
go back to reference Gore, C., C.G.B. Peterson, P. Kissen, B.M. Simpson, L.A. Lowe, A. Woodcock, and A. Custovic. 2003. Urinary eosinophilic protein X, atopy, and symptoms suggestive of allergic disease at 3 years of age. The Journal of Allergy and Clinical Immunology 112: 702–708.PubMedCrossRef Gore, C., C.G.B. Peterson, P. Kissen, B.M. Simpson, L.A. Lowe, A. Woodcock, and A. Custovic. 2003. Urinary eosinophilic protein X, atopy, and symptoms suggestive of allergic disease at 3 years of age. The Journal of Allergy and Clinical Immunology 112: 702–708.PubMedCrossRef
18.
go back to reference Ott, N.L., G.J. Gleich, E.A. Peterson, T. Fujisawa, S. Sur, and K.M. Leiferman. 1994. Assessment of eosinophil and neutrophil participation in atopic dermatitis: comparison with the IgE-mediated late-phase reaction. The Journal of Allergy and Clinical Immunology 94: 120–128.PubMedCrossRef Ott, N.L., G.J. Gleich, E.A. Peterson, T. Fujisawa, S. Sur, and K.M. Leiferman. 1994. Assessment of eosinophil and neutrophil participation in atopic dermatitis: comparison with the IgE-mediated late-phase reaction. The Journal of Allergy and Clinical Immunology 94: 120–128.PubMedCrossRef
19.
go back to reference Breuer, K., A. Kapp, and T. Werfel. 2001. Urine eosinophil protein X (EPX) is an in vitro parameter of inflammation in atopic dermatitis of the adult age. Allergy 56: 780–784.PubMedCrossRef Breuer, K., A. Kapp, and T. Werfel. 2001. Urine eosinophil protein X (EPX) is an in vitro parameter of inflammation in atopic dermatitis of the adult age. Allergy 56: 780–784.PubMedCrossRef
20.
go back to reference Carlson, M., Y. Raab, C. Peterson, R. Hallgren, and P. Venge. 1999. Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfusion. American Journal of Gastroenterology 94: 1876–1883.PubMedCrossRef Carlson, M., Y. Raab, C. Peterson, R. Hallgren, and P. Venge. 1999. Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfusion. American Journal of Gastroenterology 94: 1876–1883.PubMedCrossRef
21.
go back to reference Tischendorf, F.W., N.W. Brattig, G.D. Burchard, T. Kubica, G. Kreuzpaintner, and M. Lintzel. 1999. Eosinophils, eosinophil cationic protein and eosinophil-derived neurotoxin in serum and urine of patients with onchocerciasis coinfected with intestinal nematodes and in urinary schistosomiasis. Acta Tropica 72: 157–173.PubMedCrossRef Tischendorf, F.W., N.W. Brattig, G.D. Burchard, T. Kubica, G. Kreuzpaintner, and M. Lintzel. 1999. Eosinophils, eosinophil cationic protein and eosinophil-derived neurotoxin in serum and urine of patients with onchocerciasis coinfected with intestinal nematodes and in urinary schistosomiasis. Acta Tropica 72: 157–173.PubMedCrossRef
22.
go back to reference Tischendorf, F.W., N.W. Brattig, M. Lintzel, D.W. Buttner, G.D. Burchard, K. Bork, and M. Muller. 2000. Eosinophil granule proteins in serum and urine of patients with helminth infections and atopic dermatitis. Tropical Medicine & International Health 5: 898–905.CrossRef Tischendorf, F.W., N.W. Brattig, M. Lintzel, D.W. Buttner, G.D. Burchard, K. Bork, and M. Muller. 2000. Eosinophil granule proteins in serum and urine of patients with helminth infections and atopic dermatitis. Tropical Medicine & International Health 5: 898–905.CrossRef
23.
go back to reference Koller, D.Y., M. Nilsson, I. Enander, P. Venge, and I. Eichler. 1998. Serum eosinophil cationic protein, eosinophil protein x and eosinophil peroxidase in relation to pulmonary function in cystic fibrosis. Clinical and Experimental Allergy 28: 241–248.PubMedCrossRef Koller, D.Y., M. Nilsson, I. Enander, P. Venge, and I. Eichler. 1998. Serum eosinophil cationic protein, eosinophil protein x and eosinophil peroxidase in relation to pulmonary function in cystic fibrosis. Clinical and Experimental Allergy 28: 241–248.PubMedCrossRef
24.
go back to reference Carlson, M., L. Håkansson, M. Kämpe, G. Stålenheim, C. Peterson, and P. Venge. 1992. Degranulation of eosinophils from pollen-atopic patients with asthma is increased during pollen season. The Journal of Allergy and Clinical Immunology 89: 131–139.PubMedCrossRef Carlson, M., L. Håkansson, M. Kämpe, G. Stålenheim, C. Peterson, and P. Venge. 1992. Degranulation of eosinophils from pollen-atopic patients with asthma is increased during pollen season. The Journal of Allergy and Clinical Immunology 89: 131–139.PubMedCrossRef
25.
go back to reference Seton, K., L. Håkansson, M. Karawajczyk, and P. Venge. 2003. The stimulus-dependent release of eosinophil cationic protein and eosinophil protein x increases in apoptotic eosinophils. Scandinavian Journal of Immunology 58: 312–320.PubMedCrossRef Seton, K., L. Håkansson, M. Karawajczyk, and P. Venge. 2003. The stimulus-dependent release of eosinophil cationic protein and eosinophil protein x increases in apoptotic eosinophils. Scandinavian Journal of Immunology 58: 312–320.PubMedCrossRef
26.
go back to reference Melo, R.C.N., A.M. Dvorak, and P.F. Weller. 2010. Contributions of electron microscopy to understand secretion of immune mediators by human eosinophils. Microscopy and Microanalysis 16: 653–660.PubMedCrossRef Melo, R.C.N., A.M. Dvorak, and P.F. Weller. 2010. Contributions of electron microscopy to understand secretion of immune mediators by human eosinophils. Microscopy and Microanalysis 16: 653–660.PubMedCrossRef
27.
go back to reference Melo, R.C., L.A. Spencer, S.A. Perez, J.S. Neves, S. Bafford, E.S. Morgan, A.M. Dvorak, and P.F. Weller. 2009. Vesicle-mediated secretion of human eosinophil granule-derived major basic protein (MBP). Laboratory Investigation 89: 769–781.PubMedCrossRef Melo, R.C., L.A. Spencer, S.A. Perez, J.S. Neves, S. Bafford, E.S. Morgan, A.M. Dvorak, and P.F. Weller. 2009. Vesicle-mediated secretion of human eosinophil granule-derived major basic protein (MBP). Laboratory Investigation 89: 769–781.PubMedCrossRef
28.
go back to reference Karawajczyk, M., L. Seveus, R. Garcia, E. Bjornsson, C.G. Peterson, G.M. Roomans, and P. Venge. 2000. Piecemeal degranulation of peripheral blood eosinophils: a study of allergic subjects during and out of the pollen season. American Journal of Respiratory Cell and Molecular Biology 23: 521–529.PubMed Karawajczyk, M., L. Seveus, R. Garcia, E. Bjornsson, C.G. Peterson, G.M. Roomans, and P. Venge. 2000. Piecemeal degranulation of peripheral blood eosinophils: a study of allergic subjects during and out of the pollen season. American Journal of Respiratory Cell and Molecular Biology 23: 521–529.PubMed
29.
go back to reference Melo, R.C.N., L.A. Spencer, A.M. Dvorak, and P.F. Weller. 2008. Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule-derived cytokines and other proteins. Journal of Leukocyte Biology 83: 229–236.PubMedCrossRef Melo, R.C.N., L.A. Spencer, A.M. Dvorak, and P.F. Weller. 2008. Mechanisms of eosinophil secretion: large vesiculotubular carriers mediate transport and release of granule-derived cytokines and other proteins. Journal of Leukocyte Biology 83: 229–236.PubMedCrossRef
30.
go back to reference Melo, R.C., and P.F. Weller. 2010. Piecemeal degranulation in human eosinophils: a distinct secretion mechanism underlying inflammatory responses. Histology and Histopathology 25: 1341–1354.PubMed Melo, R.C., and P.F. Weller. 2010. Piecemeal degranulation in human eosinophils: a distinct secretion mechanism underlying inflammatory responses. Histology and Histopathology 25: 1341–1354.PubMed
31.
go back to reference Hansel, T.T., I.J.M. De Vries, T. Iff, S. Rihs, M. Wandzilak, S. Betz, K. Blaser, and C. Walker. 1991. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. Journal of Immunological Methods 145: 105–110.PubMedCrossRef Hansel, T.T., I.J.M. De Vries, T. Iff, S. Rihs, M. Wandzilak, S. Betz, K. Blaser, and C. Walker. 1991. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. Journal of Immunological Methods 145: 105–110.PubMedCrossRef
32.
go back to reference Storrie, B., and E.A. Madden. 1990. Isolation of subcellular organelles. Methods in Enzymology 182: 203–225.PubMedCrossRef Storrie, B., and E.A. Madden. 1990. Isolation of subcellular organelles. Methods in Enzymology 182: 203–225.PubMedCrossRef
33.
go back to reference Calafat, J., T.W. Kuijpers, H. Janssen, N. Borregaard, A.J. Verhoeven, and D. Roos. 1993. Evidence for small intracellular vesicles in human blood phagocytes containing cytochrome b558 and the adhesion molecule CD11b/CD18. Blood 81: 3122–3129.PubMed Calafat, J., T.W. Kuijpers, H. Janssen, N. Borregaard, A.J. Verhoeven, and D. Roos. 1993. Evidence for small intracellular vesicles in human blood phagocytes containing cytochrome b558 and the adhesion molecule CD11b/CD18. Blood 81: 3122–3129.PubMed
34.
go back to reference Peterson, C.G., I. Enander, J. Nystrand, A.S. Anderson, L. Nilsson, and P. Venge. 1991. Radioimmunoassay of human eosinophil cationic protein (ECP) by an improved method. Establishment of normal levels in serum and turnover in vivo. Clinical and Experimental Allergy 21: 561–567.PubMedCrossRef Peterson, C.G., I. Enander, J. Nystrand, A.S. Anderson, L. Nilsson, and P. Venge. 1991. Radioimmunoassay of human eosinophil cationic protein (ECP) by an improved method. Establishment of normal levels in serum and turnover in vivo. Clinical and Experimental Allergy 21: 561–567.PubMedCrossRef
35.
go back to reference Gartner, I. 1980. Separation of human eosinophils in density gradients of polyvinylpyrrolidone-coated silica gel (Percoll). Immunology 40: 133–136.PubMed Gartner, I. 1980. Separation of human eosinophils in density gradients of polyvinylpyrrolidone-coated silica gel (Percoll). Immunology 40: 133–136.PubMed
36.
go back to reference Krouwels, F.H., L.C.M. Kerstens, H.W.M. Van der Maarel, H.J. Degenhart, and H.J. Neijens. 1995. Density of eosinophils reflects activity of disease in allergic asthmatic children. Clinical and Experimental Allergy 25: 1171–1178.PubMedCrossRef Krouwels, F.H., L.C.M. Kerstens, H.W.M. Van der Maarel, H.J. Degenhart, and H.J. Neijens. 1995. Density of eosinophils reflects activity of disease in allergic asthmatic children. Clinical and Experimental Allergy 25: 1171–1178.PubMedCrossRef
37.
go back to reference Miyasato, M., S. Tsuda, T. Nakama, K. Kato, N. Kitamura, J. Nagaji, and Y. Sasai. 1996. Serum levels of eosinophil cationic protein reflect the state of in vitro degranulation of blood hypodense eosinophils in atopic dermatitis. Journal of Dermatology 23: 382–388.PubMed Miyasato, M., S. Tsuda, T. Nakama, K. Kato, N. Kitamura, J. Nagaji, and Y. Sasai. 1996. Serum levels of eosinophil cationic protein reflect the state of in vitro degranulation of blood hypodense eosinophils in atopic dermatitis. Journal of Dermatology 23: 382–388.PubMed
38.
go back to reference Hoffmann, H.J., T. Bjerke, M. Karawajczyk, R. Dahl, M.A. Knepper, and S. Nielsen. 2001. SNARE proteins are critical for regulated exocytosis of ECP from human eosinophils. Biochemical and Biophysical Research Communications 282: 194–199.PubMedCrossRef Hoffmann, H.J., T. Bjerke, M. Karawajczyk, R. Dahl, M.A. Knepper, and S. Nielsen. 2001. SNARE proteins are critical for regulated exocytosis of ECP from human eosinophils. Biochemical and Biophysical Research Communications 282: 194–199.PubMedCrossRef
39.
go back to reference Bjerrum, O.W., and N. Borregaard. 1989. Dual granule localization of the dormant NADPH oxidase and cytochrome b559 in human neutrophils. European Journal of Haematology 43: 67–77.PubMedCrossRef Bjerrum, O.W., and N. Borregaard. 1989. Dual granule localization of the dormant NADPH oxidase and cytochrome b559 in human neutrophils. European Journal of Haematology 43: 67–77.PubMedCrossRef
40.
go back to reference Metcalfe, D.D., J. Litvin, and S.I. Wasserman. 1982. The isolation, identification and characterization of sulfated glycosaminoglycans synthesized in vitro by human eosinophils. Biochimica et Biophysica Acta 715: 196–204.PubMedCrossRef Metcalfe, D.D., J. Litvin, and S.I. Wasserman. 1982. The isolation, identification and characterization of sulfated glycosaminoglycans synthesized in vitro by human eosinophils. Biochimica et Biophysica Acta 715: 196–204.PubMedCrossRef
41.
go back to reference Rothenberg, M.E., J.L. Pomerantz, W.F. Owen, S. Avraham, R.J. Soberman, K.F. Austen, and R.L. Stevens. 1988. Characterization of a human eosinophil proteoglycan, and augmentation of its biosynthesis and size by interleukin 3, interleukin 5, and granulocyte/macrophage colony stimulating factor. Journal of Biological Chemistry 263: 13901–13908.PubMed Rothenberg, M.E., J.L. Pomerantz, W.F. Owen, S. Avraham, R.J. Soberman, K.F. Austen, and R.L. Stevens. 1988. Characterization of a human eosinophil proteoglycan, and augmentation of its biosynthesis and size by interleukin 3, interleukin 5, and granulocyte/macrophage colony stimulating factor. Journal of Biological Chemistry 263: 13901–13908.PubMed
42.
go back to reference Zhang, H., X. Gao, C. Weng, and Z. Xu. 2008. Interaction between angiogenin and fibulin 1: evidence and implication. Acta Biochimica et Biophysica Sinica (Shanghai) 40: 375–380.CrossRef Zhang, H., X. Gao, C. Weng, and Z. Xu. 2008. Interaction between angiogenin and fibulin 1: evidence and implication. Acta Biochimica et Biophysica Sinica (Shanghai) 40: 375–380.CrossRef
43.
go back to reference Melo, R.C., S.A. Perez, L.A. Spencer, A.M. Dvorak, and P.F. Weller. 2005. Intragranular vesiculotubular compartments are involved in piecemeal degranulation by activated human eosinophils. Traffic 6: 866–879.PubMedCrossRef Melo, R.C., S.A. Perez, L.A. Spencer, A.M. Dvorak, and P.F. Weller. 2005. Intragranular vesiculotubular compartments are involved in piecemeal degranulation by activated human eosinophils. Traffic 6: 866–879.PubMedCrossRef
44.
go back to reference Melo, R.C., L.A. Spencer, S.A. Perez, I. Ghiran, A.M. Dvorak, and P.F. Weller. 2005. Human eosinophils secrete preformed, granule-stored interleukin-4 through distinct vesicular compartments. Traffic 6: 1047–1057.PubMedCrossRef Melo, R.C., L.A. Spencer, S.A. Perez, I. Ghiran, A.M. Dvorak, and P.F. Weller. 2005. Human eosinophils secrete preformed, granule-stored interleukin-4 through distinct vesicular compartments. Traffic 6: 1047–1057.PubMedCrossRef
45.
go back to reference Moqbel, R., and J.J. Coughlin. 2006. Differential secretion of cytokines. Sci. STKE 2006: pe26. Moqbel, R., and J.J. Coughlin. 2006. Differential secretion of cytokines. Sci. STKE 2006: pe26.
Metadata
Title
An Extragranular Compartment of Blood Eosinophils Contains Eosinophil Protein X/Eosinophil-Derived Neurotoxin (EPX/EDN)
Authors
Malgorzata Karawajczyk
Christer G. B. Peterson
Per Venge
Rodolfo C. Garcia
Publication date
01-04-2013
Publisher
Springer US
Published in
Inflammation / Issue 2/2013
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-012-9549-z

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