Eosinophil granule proteins: Form and function

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17406-17415

  Acharya, K Ravi ^a   Ackerman, Steven J ^b  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DISEASES; GRANULATION; MAMMALS; MOLECULAR BIOLOGY; T-CELLS; TISSUE;

ADAPTIVE IMMUNITY; AIRWAY INFLAMMATION; AIRWAY REMODELING; CATIONIC PROTEINS; EOSINOPHIL-GRANULE; IMMUNOMODULATORY; MOLECULAR ASPECTS; STRUCTURE-FUNCTION RELATIONSHIP;

PROTEINS;

CHARCOT LEYDEN CRYSTAL PROTEIN; EOSINOPHIL CATIONIC PROTEIN; EOSINOPHIL GRANULE PROTEIN; EOSINOPHIL PEROXIDASE; EOSINOPHIL PROTEIN X; GALECTIN; MAJOR BASIC PROTEIN; MAJOR BASIC PROTEIN 1; MAJOR BASIC PROTEIN 2; UNCLASSIFIED DRUG;

ASTHMA; CRYSTAL STRUCTURE; EOSINOPHIL; HUMAN; IMMUNOBIOLOGY; LUNG DISEASE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; SEQUENCE ANALYSIS; SHORT SURVEY; STRUCTURE ACTIVITY RELATION;

ASTHMA; CRYSTAL STRUCTURE; ENZYME STRUCTURE; EOSINOPHIL; EOSINOPHIL GRANULE PROTEINS; INFLAMMATION;

ADAPTIVE IMMUNITY; ANIMALS; ASTHMA; DIABETES MELLITUS; EOSINOPHIL MAJOR BASIC PROTEIN; EOSINOPHIL PEROXIDASE; EOSINOPHILS; HUMANS; LUNG; MICE; MICE, KNOCKOUT; STRUCTURE-ACTIVITY RELATIONSHIP; TH2 CELLS;

EID: 84903454996     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R113.546218     Document Type: Short Survey

References (100)

1. Rosenberg, H. F., Dyer, K. D., and Foster, P. S. (2013) Eosinophils: changing perspectives in health and disease. Nat. Rev. Immunol. 13, 9-22
2. Hogan, S. P., Rosenberg, H. F., Moqbel, R., Phipps, S., Foster, P. S., Lacy, P., Kay, A. B., and Rothenberg, M. E. (2008) Eosinophils: biological properties and role in health and disease. Clin. Exp. Allergy 38, 709-750 (Pubitemid 351550670)
3. Lee, J. J., Dimina, D., Macias, M. P., Ochkur, S. I., McGarry, M. P., O'Neill, K. R., Protheroe, C., Pero, R., Nguyen, T., Cormier, S. A., Lenkiewicz, E., Colbert, D., Rinaldi, L., Ackerman, S. J., Irvin, C. G., and Lee, N. A. (2004) Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305, 1773-1776 (Pubitemid 39249644)
4. Humbles, A. A., Lloyd, C. M., McMillan, S. J., Friend, D. S., Xanthou, G., McKenna, E. E., Ghiran, S., Gerard, N. P., Yu, C., Orkin, S. H., and Gerard, C. (2004) A critical role for eosinophils in allergic airways remodeling. Science 305, 1776-1779 (Pubitemid 39249645)
5. Gleich, G. J., Adolphson, C. R., and Kita, H., (eds) (2000) Asthma and Rhinitis, Vol. 1, 2nd Ed., Blackwell Science Ltd., Oxford, England
6. Jacobsen, E. A., Lesuer, W. E., Willetts, L., Zellner, K. R., Mazzolini, K., Antonios, N., Beck, B., Protheroe, C., Ochkur, S. I., Colbert, D., Lacy, P., Moqbel, R., Appleton, J., Lee, N. A., and Lee, J. J. (2014) Eosinophil activities modulate the immune/inflammatory character of allergic respiratory responses in mice. Allergy 69, 315-327
7. Denzler, K. L., Farmer, S. C., Crosby, J. R., Borchers, M., Cieslewicz, G., Larson, K. A., Cormier-Regard, S., Lee, N. A., and Lee, J. J. (2000) Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J. Immunol. 165, 5509-5517
8. Specht, S., Saeftel, M., Arndt, M., Endl, E., Dubben, B., Lee, N. A., Lee, J. J., and Hoerauf, A. (2006) Lack of eosinophil peroxidase or major basic protein impairs defense against murine filarial infection. Infect. Immun. 74, 5236-5243 (Pubitemid 44300442)
9. Doyle, A. D., Jacobsen, E. A., Ochkur, S. I., McGarry, M. P., Shim, K. G., Nguyen, D. T., Protheroe, C., Colbert, D., Kloeber, J., Neely, J., Shim, K. P., Dyer, K. D., Rosenberg, H. F., Lee, J. J., and Lee, N. A. (2013) Expression of the secondary granule proteins major basic protein 1 (MBP-1) and eosinophil peroxidase (EPX) is required for eosinophilopoiesis in mice. Blood 122, 781-790
10. Fabre, V., Beiting, D. P., Bliss, S. K., Gebreselassie, N. G., Gagliardo, L. F., Lee, N. A., Lee, J. J., and Appleton, J. A. (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. J. Immunol. 182, 1577-1583
11. Gebreselassie, N. G., Moorhead, A. R., Fabre, V., Gagliardo, L. F., Lee, N. A., Lee, J. J., and Appleton, J. A. (2012) Eosinophils preserve parasitic nematode larvae by regulating local immunity. J. Immunol. 188, 417-425
12. Nair, P., Pizzichini, M. M., Kjarsgaard, M., Inman, M. D., Efthimiadis, A., Pizzichini, E., Hargreave, F. E., and O'Byrne, P. M. (2009) Mepolizumab for prednisone-dependent asthma with sputum eosinophilia. N. Engl. J. Med. 360, 985-993
13. Rothenberg, M. E., Klion, A. D., Roufosse, F. E., Kahn, J. E., Weller, P. F., Simon, H. U., Schwartz, L. B., Rosenwasser, L. J., Ring, J., Griffin, E. F., Haig, A. E., Frewer, P. I., Parkin, J. M., and Gleich, G. J. (2008) Treatment of patients with the hypereosinophilic syndrome with mepolizumab. N. Engl. J. Med. 358, 1215-1228 (Pubitemid 351439223)
14. Leiferman, K. M., Gleich, G. J., Kephart, G. M., Haugen, H. S., Hisamatsu, K., Proud, D., Lichtenstein, L. M., and Ackerman, S. J. (1986) Differences between basophils and mast cells: failure to detect Charcot-Leyden crystal protein (lysophospholipase) and eosinophil granule major basic protein in human mast cells. J. Immunol. 136, 852-855 (Pubitemid 16146365)
15. Ackerman, S. J., Kephart, G. M., Habermann, T. M., Greipp, P. R., and Gleich, G. J. (1983) Localization of eosinophil granule major basic protein in human basophils. J. Exp. Med. 158, 946-961 (Pubitemid 13051356)
16. Abu-Ghazaleh, R. I., Dunnette, S. L., Loegering, D. A., Checkel, J. L., Kita, H., Thomas, L. L., and Gleich, G. J. (1992) Eosinophil granule proteins in peripheral blood granulocytes. J. Leukoc. Biol. 52, 611-618 (Pubitemid 23016034)
17. Golightly, L. M., Thomas, L. L., Dvorak, A. M., and Ackerman, S. J. (1992) Charcot-Leyden crystal protein in the degranulation and recovery of activated basophils. J. Leukoc. Biol. 51, 386-392
18. Ackerman, S. J., Weil, G. J., and Gleich, G. J. (1982) Formation of Charcot-Leyden crystals by human basophils. J. Exp. Med. 155, 1597-1609 (Pubitemid 12074201)
19. Rosenberg, H. F., Tenen, D. G., and Ackerman, S. J. (1989) Molecular cloning of the human eosinophil-derived neurotoxin: a member of the ribonuclease gene family. Proc. Natl. Acad. Sci. U.S.A. 86, 4460-4464 (Pubitemid 19164574)
20. Rosenberg, H. F., Ackerman, S. J., and Tenen, D. G. (1989) Human eosinophil cationic protein: molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. J. Exp. Med. 170, 163-176 (Pubitemid 19179702)
21. Sur, S., Glitz, D. G., Kita, H., Kujawa, S. M., Peterson, E. A., Weiler, D. A., Kephart, G. M., Wagner, J. M., George, T. J., Gleich, G. J., and Leiferman, K. M. (1998) Localization of eosinophil-derived neurotoxin and eosinophil cationic protein in neutrophilic leukocytes. J. Leukoc. Biol. 63, 715-722 (Pubitemid 28274833)
22. Sorrentino, S., Glitz, D. G., Hamann, K. J., Loegering, D. A., Checkel, J. L., and Gleich, G. J. (1992) Eosinophil-derived neurotoxin and human liver ribonuclease: identity of structure and linkage of neurotoxicity to nuclease activity. J. Biol. Chem. 267, 14859-14865
23. Kubach, J., Lutter, P., Bopp, T., Stoll, S., Becker, C., Huter, E., Richter, C., Weingarten, P., Warger, T., Knop, J., Müllner, S., Wijdenes, J., Schild, H., Schmitt, E., and Jonuleit, H. (2007) Human CD4+CD25+ regulatory T cells: proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function. Blood 110, 1550-1558 (Pubitemid 47443971)
24. Schmetterer, K. G., Neunkirchner, A., and Pickl, W. F. (2012) Naturally occurring regulatory T cells: markers, mechanisms, and manipulation. FASEB J. 26, 2253-2276
25. Wang, Y. H., Ito, T., Wang, Y. H., Homey, B., Watanabe, N., Martin, R., Barnes, C. J., McIntyre, B. W., Gilliet, M., Kumar, R., Yao, Z., and Liu, Y. J. (2006) Maintenance and polarization of human TH2 central memory T cells by thymic stromal lymphopoietin-activated dendritic cells. Immunity 24, 827-838 (Pubitemid 43867361)
26. Yousefi, S., Simon, D., and Simon, H. U. (2012) Eosinophil extracellular DNA traps: molecular mechanisms and potential roles in disease. Curr. Opin. Immunol. 24, 736-739
27. Yousefi, S., Gold, J. A., Andina, N., Lee, J. J., Kelly, A. M., Kozlowski, E., Schmid, I., Straumann, A., Reichenbach, J., Gleich, G. J., and Simon, H. U. (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat. Med. 14, 949-953
28. Simon, D., Simon, H. U., and Yousefi, S. (2013) Extracellular DNA traps in allergic, infectious, and autoimmune diseases. Allergy 68, 409-416
29. Dworski, R., Simon, H. U., Hoskins, A., and Yousefi, S. (2011) Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways. J. Allergy Clin. Immunol. 127, 1260-1266
30. Simon, D., Hoesli, S., Roth, N., Staedler, S., Yousefi, S., and Simon, H. U. (2011) Eosinophil extracellularDNAtraps in skin diseases. J. Allergy Clin. Immunol. 127, 194-199
31. Morshed, M., Yousefi, S., Stöckle, C., Simon, H. U., and Simon, D. (2012) Thymic stromal lymphopoietin stimulates the formation of eosinophil extracellular traps. Allergy 67, 1127-1137
32. Gleich, G. J., Adolphson, C. R., and Leiferman, K. M. (1993) The biology of the eosinophilic leukocyte. Annu. Rev. Med. 44, 85-101 (Pubitemid 23117851)
33. Gundel, R. H., Letts, L. G., and Gleich, G. J. (1991) Human eosinophil major basic protein induces airway constriction and airway hyperresponsiveness in primates. J. Clin. Invest. 87, 1470-1473
34. Thomas, L. L., Xu, W., and Ardon, T. T. (2002) Immobilized lactoferrin is a stimulus for eosinophil activation, J. Immunol. 169, 993-999 (Pubitemid 34753458)
35. Temkin, V., Aingorn, H., Puxeddu, I., Goldshmidt, O., Zcharia, E., Gleich, G. J., Vlodavsky, I., and Levi-Schaffer, F. (2004) Eosinophil major basic protein: first identified natural heparanase-inhibiting protein. J. Allergy Clin. Immunol. 113, 703-709 (Pubitemid 38530427)
36. Pégorier, S., Wagner, L. A., Gleich, G. J., and Pretolani, M. (2006) Eosinophil-derived cationic proteins activate the synthesis of remodeling factors by airway epithelial cells. J. Immunol. 177, 4861-4869
37. Wehling-Henricks, M., Sokolow, S., Lee, J. J., Myung, K. H., Villalta, S. A., and Tidball, J. G. (2008) Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum. Mol. Genet. 17, 2280-2292
38. Denzler, K. L., Borchers, M. T., Crosby, J. R., Cieslewicz, G., Hines, E. M., Justice, J. P., Cormier, S. A., Lindenberger, K. A., Song, W., Wu, W., Hazen, S. L., Gleich, G. J., Lee, J. J., and Lee, N. A. (2001) Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J. Immunol. 167, 1672-1682 (Pubitemid 32703170)
39. Ackerman, S. J. (2013) To be, or not to be, an eosinophil: that is the ???. Blood 122, 621-623
40. Plager, D. A., Loegering, D. A., Weiler, D. A., Checkel, J. L., Wagner, J. M., Clarke, N. J., Naylor, S., Page, S. M., Thomas, L. L., Akerblom, I., Cocks, B., Stuart, S., and Gleich, G. J. (1999) A novel and highly divergent homolog of human eosinophil granule major basic protein. J. Biol. Chem. 274, 14464-14473
41. Oxvig, C., Gleich, G. J., and Sottrup-Jensen, L. (1994) Localization of disulfide bridges and free sulfhydryl groups in human eosinophil granule major basic protein. FEBS Lett. 341, 213-217 (Pubitemid 24102684)
42. Patthy, L. (1989) Homology of cytotoxic protein of eosinophilic leukocytes with IgE receptor Fcε RII: implications for its structure and function. Mol. Immunol. 26, 1151-1154
43. Swaminathan, G. J., Weaver, A. J., Loegering, D. A., Checkel, J. L., Leonidas, D. D., Gleich, G. J., and Acharya, K. R. (2001) Crystal structure of the eosinophil major basic protein at 1.8 Å: an atypical lectin with a paradigm shift in specificity. J. Biol. Chem. 276, 26197-26203
44. Swaminathan, G. J., Myszka, D. G., Katsamba, P. S., Ohnuki, L. E., Gleich, G. J., and Acharya, K. R. (2005) Eosinophil-granule major basic protein, a C-type lectin, binds heparin. Biochemistry 44, 14152-14158 (Pubitemid 41533040)
45. Jacoby, D. B., Gleich, G. J., and Fryer, A. D. (1993) Human eosinophil major basic protein is an endogenous allosteric antagonist at the inhibitory muscarinic M2 receptor. J. Clin. Invest. 91, 1314-1318 (Pubitemid 23127327)
46. Evans, C. M., Fryer, A. D., Jacoby, D. B., Gleich, G. J., and Costello, R. W. (1997) Pretreatment with antibody to eosinophil major basic protein prevents hyperresponsiveness by protecting neuronal M2 muscarinic receptors in antigen-challenged guinea pigs. J. Clin. Invest. 100, 2254-2262 (Pubitemid 27500148)
47. Fryer, A. D., and Jacoby, D. B. (1992) Function of pulmonary M2 muscarinic receptors in antigen-challenged guinea pigs is restored by heparin and poly-L-glutamate. J. Clin. Invest. 90, 2292-2298 (Pubitemid 23010044)
48. Yost, B. L., Gleich, G. J., and Fryer, A. D. (1999) Ozone-induced hyperresponsiveness and blockade of M2 muscarinic receptors by eosinophil major basic protein. J. Appl Physiol. 87, 1272-1278 (Pubitemid 29483108)
49. Ackerman, S. J., Loegering, D. A., Venge, P., Olsson, I., Harley, J. B., Fauci, A. S., and Gleich, G. J. (1983) Distinctive cationic proteins of the human eosinophil granule: major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin. J. Immunol. 131, 2977-2982 (Pubitemid 14207333)
50. Hamann, K. J., Barker, R. L., Loegering, D. A., and Gleich, G. J. (1987) Comparative toxicity of purified human eosinophil granule proteins for newborn larvae of Trichinella spiralis. J. Parasitol. 73, 523-529
51. Domachowske, J. B., Dyer, K. D., Bonville, C. A., and Rosenberg, H. F. (1998) Recombinant human eosinophil-derived neurotoxin/RNase 2 functions as an effective antiviral agent against respiratory syncytial virus, J. Infect. Dis. 177, 1458-1464 (Pubitemid 28243566)
52. Fredens, K., Dahl, R., and Venge, P. (1982) The Gordon phenomenon induced by the eosinophil cationic protein and eosinophil protein X. J. Allergy Clin. Immunol. 70, 361-366 (Pubitemid 13233284)
53. Gleich, G. J., Loegering, D. A., Bell, M. P., Checkel, J. L., Ackerman, S. J., and McKean, D. J. (1986) Biochemical and functional similarities between human eosinophil-derived neurotoxin and eosinophil cationic protein: homology with ribonuclease. Proc. Natl. Acad. Sci. U.S.A. 83, 3146-3150 (Pubitemid 16042993)
54. Newton, D. L., Nicholls, P. J., Rybak, S. M., and Youle, R. J. (1994) Expression and characterization of recombinant human eosinophil-derived neurotoxin and eosinophil-derived neurotoxin-anti-transferrin receptor sFv. J. Biol. Chem. 269, 26739-26745 (Pubitemid 24332866)
55. Hofsteenge, J., Müller, D. R., de Beer, T., Löffler, A., Richter, W. J., and Vliegenthart, J. F. (1994) New type of linkage between a carbohydrate and a protein: C-glycosylation of a specific tryptophan residue in human RNase Us, Biochemistry 33, 13524-13530
56. Hamann, K. J., Gleich, G. J., Checkel, J. L., Loegering, D. A., McCall, J. W., and Barker, R. L. (1990) In vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. J. Immunol. 144, 3166-3173 (Pubitemid 20149496)
57. Yang, D., Chen, Q., Rosenberg, H. F., Rybak, S. M., Newton, D. L., Wang, Z. Y., Fu, Q., Tchernev, V. T., Wang, M., Schweitzer, B., Kingsmore, S. F., Patel, D. D., Oppenheim, J. J., and Howard, O. M. (2004) Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation, J. Immunol. 173, 6134-6142 (Pubitemid 39487770)
58. Yang, D., Chen, Q., Su, S. B., Zhang, P., Kurosaka, K., Caspi, R. R., Michalek, S. M., Rosenberg, H. F., Zhang, N., and Oppenheim, J. J. (2008) Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J. Exp. Med. 205, 79-90 (Pubitemid 351185717)
59. Leonidas, D. D., Boix, E., Prill, R., Suzuki, M., Turton, R., Minson, K., Swaminathan, G. J., Youle, R. J., and Acharya, K. R. (2001) Mapping the ribonucleolytic active site of eosinophil-derived neurotoxin (EDN): high resolution crystal structures of EDN complexes with adenylic nucleotide inhibitors. J. Biol. Chem. 276, 15009-15017
60. Boix, E., Leonidas, D. D., Nikolovski, Z., Nogués, M. V., Cuchillo, C. M., and Acharya, K. R. (1999) Crystal structure of eosinophil cation protein at 2.4 Å resolution. Biochemistry 38, 16794-16801
61. Boix, E., Nikolovski, Z., Moiseyev, G. P., Rosenberg, H. F., Cuchillo, C. M., and Nogués, M. V. (1999) Kinetic and product distribution analysis of human eosinophil cationic protein indicates a subsite arrangement that favors exonuclease-type activity. J. Biol. Chem. 274, 15605-15614
62. Larson K. A., Olson, E. V., Madden, B. J., Gleich, G. J., Lee, N. A., and Lee, J. J. (1996) Two highly homologous ribonuclease genes expressed in mouse eosinophils identify a larger subgroup of the mammalian ribonuclease superfamily. Proc. Natl. Acad. Sci. U.S.A. 93, 12370-12375 (Pubitemid 26367150)
63. Zhang, J., Dyer, K. D., and Rosenberg, H. F. (2000) Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc. Natl. Acad. Sci. U.S.A. 97, 4701-4706 (Pubitemid 30238621)
64. Rosenberg, H. F., and Domachowske, J. B. (2001) Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. J. Leukoc. Biol. 70, 691-698 (Pubitemid 33127003)
65. Boix, E., Carreras, E., Nikolovski, Z., Cuchillo, C. M., and Nogués, M. V. (2001) Identification and characterization of human eosinophil cationic protein by an epitope-specific antibody, J Leukoc. Biol 69, 1027-1035 (Pubitemid 32577907)
66. Rosenberg, H. F. (1995) Recombinant human eosinophil cationic protein: ribonuclease activity is not essential for cytotoxicity. J. Biol. Chem. 270, 7876-7881
67. Domachowske, J. B., Dyer, K. D., Adams, A. G., Leto, T. L., and Rosenberg, H. F. (1998) Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res. 26, 3358-3363 (Pubitemid 28321399)
68. Hamann, K. J., Ten, R. M., Loegering, D. A., Jenkins, R. B., Heise, M. T., Schad, C. R., Pease, L. R., Gleich, G. J., and Barker, R. L. (1990) Structure and chromosome localization of the human eosinophil-derived neurotoxin and eosinophil cationic protein genes: evidence for intronless coding sequences in the ribonuclease gene superfamily. Genomics 7, 535-546 (Pubitemid 20244457)
69. Mohan, C. G., Boix, E., Evans, H. R., Nikolovski, Z., Nogués, M. V., Cuchillo, C. M., and Acharya, K. R. (2002) The crystal structure of eosinophil cationic protein in complex with 2′,5′-ADP at 2.0 Å resolution reveals the details of the ribonucleolytic active site. Biochemistry 41, 12100-12106
70. Boix, E., Salazar, V. A., Torrent, M., Pulido, D., Nogués, M. V., and Moussaoui, M. (2012) Structural determinants of the eosinophil cationic protein antimicrobial activity. Biol. Chem. 393, 801-815
71. Sánchez, D., Moussaoui, M., Carreras, E., Torrent, M., Nogués, V., and Boix, E. (2011) Mapping the eosinophil cationic protein antimicrobial activity by chemical and enzymatic cleavage. Biochimie 93, 331-338
72. Svensson, L., and Wennerås, C. (2005) Human eosinophils selectively recognize and become activated by bacteria belonging to different taxonomic groups. Microbes Infect. 7, 720-728
73. Torrent, M., Pulido, D., Nogués, M. V., and Boix, E. (2012) Exploring new biological functions of amyloids: bacteria cell agglutination mediated by host protein aggregation. PLoS Pathog. 8, e1003005
74. Torrent, M., Pulido, D., de la Torre, B. G., García-Mayoral, M. F., Nogués, M. V., Bruix, M., Andreu, D., and Boix, E. (2011) Refining the eosinophil cationic protein antibacterial pharmacophore by rational structure minimization. J. Med. Chem. 54, 5237-5244
75. Pulido, D., Torrent, M., Andreu, D., Nogués, M. V., and Boix, E. (2013) Two human host defense ribonucleases against mycobacteria, the eosinophil cationic protein (RNase 3) and RNase 7. Antimicrob. Agents. Chemother. 57, 3797-3805
76. Trulson, A., Byström, J., Engström, A., Larsson, R., and Venge, P. (2007) The functional heterogeneity of eosinophil cationic protein is determined by a gene polymorphism and post-translational modifications. Clin. Exp. Allergy 37, 208-218
77. Rubin, J., Zagai, U., Blom, K., Trulson, A., Engström, A., and Venge, P. (2009) The coding ECP 434(G>C) gene polymorphism determines the cytotoxicity of ECP but has minor effects on fibroblast-mediated gel contraction and no effect on RNase activity. J. Immunol. 183, 445-451
78. Eriksson, J., Reimert, C. M., Kabatereine, N. B., Kazibwe, F., Ireri, E., Kadzo, H., Eltahir, H. B., Mohamed, A. O., Vennervald, B. J., and Venge, P. (2007) The 434(G>C) polymorphism within the coding sequence of eosinophil cationic protein (ECP) correlates with the natural course of Schistosoma mansoni infection. Int. J. Parasitol. 37, 1359-1366 (Pubitemid 47285103)
79. Blom, K., Rubin, J., Halfvarson, J., Törkvist, L., Rönnblom, A., Sangfelt, P., Lördal, M., Jönsson, U. B., Sjöqvist, U., Håkansson, L. D., Venge, P., and Carlson, M. (2012) Eosinophil associated genes in the inflammatory bowel disease 4 region: correlation to inflammatory bowel disease revealed. World J. Gastroenterol. 18, 6409-6419; discussion p 6417-6418
80. Jönsson, U. B., Byström, J., Stålenheim, G., and Venge, P. (2002) Polymorphism of the eosinophil cationic protein-gene is related to the expression of allergic symptoms. Clin. Exp. Allergy 32, 1092-1095
81. Jönsson, U. B., Håkansson, L. D., Jõgi, R., Janson, C., and Venge, P. (2010) Associations of ECP (eosinophil cationic protein)-gene polymorphisms to allergy, asthma, smoke habits and lung function in two Estonian and Swedish sub cohorts of the ECRHS II study. BMC Pulm. Med. 10, 36
82. Woschnagg, C., Rubin, J., and Venge, P. (2009) Eosinophil cationic protein (ECP) is processed during secretion. J. Immunol. 183, 3949-3954
83. Lacy, P., Abdel-Latif, D., Steward, M., Musat-Marcu, S., Man, S. F., and Moqbel, R. (2003) Divergence of mechanisms regulating respiratory burst in blood and sputum eosinophils and neutrophils from atopic subjects. J. Immunol. 170, 2670-2679 (Pubitemid 36245660)
84. Wang, J. G., Mahmud, S. A., Thompson, J. A., Geng, J. G., Key, N. S., and Slungaard, A. (2006) The principal eosinophil peroxidase product, HOSCN, is a uniquely potent phagocyte oxidant inducer of endothelial cell tissue factor activity: a potential mechanism for thrombosis in eosinophilic inflammatory states. Blood 107, 558-565 (Pubitemid 43076379)
85. Wang, J. G., Mahmud, S. A., Nguyen, J., and Slungaard, A. (2006) Thiocyanate-dependent induction of endothelial cell adhesion molecule expression by phagocyte peroxidases: a novel HOSCN-specific oxidant mechanism to amplify inflammation. J. Immunol. 177, 8714-8722 (Pubitemid 44893837)
86. Auriault, C., Capron, M., and Capron, A. (1982) Activation of rat and human eosinophils by soluble factor(s) released by Schistosoma mansoni schistosomula. Cell. Immunol. 66, 59-69 (Pubitemid 12185996)
87. Locksley, R. M., Wilson, C. B., and Klebanoff, S. J. (1982) Role for endogenous and acquired peroxidase in the toxoplasmacidal activity of murine and human mononuclear phagocytes. J. Clin. Invest. 69, 1099-1111 (Pubitemid 12115674)
88. Henderson, W. R., Jörg, A., and Klebanoff, S. J. (1982) Eosinophil peroxidase-mediated inactivation of leukotrienes B4, C4, and D4. J. Immunol. 128, 2609-2613
89. Henderson, W. R., Jong, E. C., and Klebanoff, S. J. (1980) Binding of eosinophil peroxidase to mast cell granules with retention of peroxidatic activity. J. Immunol. 124, 1383-1388 (Pubitemid 10062810)
90. Ulrich, M., Petre, A., Youhnovski, N., Prömm, F., Schirle, M., Schumm, M., Pero, R. S., Doyle, A., Checkel, J., Kita, H., Thiyagarajan, N., Acharya, K. R., Schmid-Grendelmeier, P., Simon, H. U., Schwarz, H., Tsutsui, M., Shimokawa, H., Bellon, G., Lee, J. J., Przybylski, M., and Döring, G. (2008) Post-translational tyrosine nitration of eosinophil granule toxins mediated by eosinophil peroxidase. J. Biol. Chem. 283, 28629-28640
91. Ackerman, S. J., Corrette, S. E., Rosenberg, H. F., Bennett, J. C., Mastrianni, D. M., Nicholson-Weller, A., Weller, P. F., Chin, D. T., and Tenen, D. G. (1993) Molecular cloning and characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase): similarities to IgE binding proteins and the S-type animal lectin superfamily. J. Immunol. 150, 456-468 (Pubitemid 23133621)
92. Weller, P. F., Bach, D. S., and Austen, K. F. (1984) Biochemical characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase). J. Biol. Chem. 259, 15100-15105 (Pubitemid 15191308)
93. Leonidas, D. D., Elbert, B. L., Zhou, Z., Leffler, H., Ackerman, S. J., and Acharya, K. R. (1995) Crystal structure of human Charcot-Leyden crystal protein, an eosinophil lysophospholipase, identifies it as a new member of the carbohydrate-binding family of galectins. Structure 3, 1379-1393 (Pubitemid 3012269)
94. Dyer, K. D., Handen, J. S., and Rosenberg, H. F. (1997) The genomic structure of the human Charcot-Leyden crystal protein gene is analogous to those of the galectin genes. Genomics 40, 217-221 (Pubitemid 27124082)
95. Ackerman, S. J., Liu, L., Kwatia, M. A., Savage, M. P., Leonidas, D. D., Swaminathan, G. J., and Acharya, K. R. (2002) Charcot-Leyden crystal protein (galectin-10) is not a dual function galectin with lysophospholipase activity but binds a lysophospholipase inhibitor in a novel structural fashion. J. Biol. Chem. 277, 14859-14868 (Pubitemid 34952559)
96. Swaminathan, G. J., Leonidas, D. D., Savage, M. P., Ackerman, S. J., and Acharya, K. R. (1999) Selective recognition of mannose by the human eosinophil Charcot-Leyden crystal protein (galectin-10): a crystallographic study at 1.8 Å resolution. Biochemistry 38, 13837-13843 (Pubitemid 29504214)
97. Furuta, G. T., Kagalwalla, A. F., Lee, J. J., Alumkal, P., Maybruck, B. T., Fillon, S., Masterson, J. C., Ochkur, S., Protheroe, C., Moore, W., Pan, Z., Amsden, K., Robinson, Z., Capocelli, K., Mukkada, V., Atkins, D., Fleischer, D., Hosford, L., Kwatia, M. A., Schroeder, S., Kelly, C., Lovell, M., Melin-Aldana, H., and Ackerman, S. J. (2013) The oesophageal string test: a novel, minimally invasive method measures mucosal inflammation in eosinophilic oesophagitis. Gut 62, 1395-1405
98. Chua, J. C., Douglass, J. A., Gillman, A., O'Hehir, R. E., and Meeusen, E. N. (2012) Galectin-10, a potential biomarker of eosinophilic airway inflammation. PLoS One 7, e42549
99. Bryborn, M., Halldén, C., Säll, T., and Cardell, L. O. (2010) CLC: a novel susceptibility gene for allergic rhinitis? Allergy 65, 220-228
100. Ghafouri, B., Irander, K., Lindbom, J., Tagesson, C., and Lindahl, M. (2006) Comparative proteomics of nasal fluid in seasonal allergic rhinitis. J. Proteome Res. 5, 330-338 (Pubitemid 43222301)