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Review Article

Antimicrobial activity of human eosinophil granule proteins: involvement in host defence against pathogens

&
Pages 168-181 | Received 06 Sep 2011, Accepted 28 Nov 2011, Published online: 13 Jan 2012

References

  • Abu-Ghazaleh RI, Dunnette SL, Loegering DA, Checkel JL, Kita H, Thomas LL, Gleich GJ. (1992). Eosinophil granule proteins in peripheral blood granulocytes. J Leukoc Biol, 52, 611–618.
  • Ackerman SJ, Kephart GM, Habermann TM, Greipp PR, Gleich GJ. (1983). Localization of eosinophil granule major basic protein in human basophils. J Exp Med, 158, 946–961.
  • Ackerman SJ, Gleich GJ, Loegering DA, Richardson BA, Butterworth AE. (1985). Comparative toxicity of purified human eosinophil granule cationic proteins for schistosomula of Schistosoma mansoni. Am J Trop Med Hyg, 34, 735–745.
  • Adamko DJ, Yost BL, Gleich GJ, Fryer AD, Jacoby DB. (1999). Ovalbumin sensitization changes the inflammatory response to subsequent parainfluenza infection. Eosinophils mediate airway hyperresponsiveness, m(2) muscarinic receptor dysfunction, and antiviral effects. J Exp Med, 190, 1465–1478.
  • Agosti JM, Altman LC, Ayars GH, Loegering DA, Gleich GJ, Klebanoff SJ. (1987). The injurious effect of eosinophil peroxidase, hydrogen peroxide, and halides on pneumocytes in vitro. J Allergy Clin Immunol, 79, 496–504.
  • Aydemir SA, Tekin IO, Numanoglu G, Borazan A, Ustundag Y. (2004). Eosinophil infiltration, gastric juice and serum eosinophil cationic protein levels in Helicobacter pylori-associated chronic gastritis and gastric ulcer. Mediators Inflamm, 13, 369–372.
  • Barker RL, Gleich GJ, Pease LR. (1988). Acidic precursor revealed in human eosinophil granule major basic protein cDNA. J Exp Med, 168, 1493–1498.
  • Barker RL, Loegering DA, Ten RM, Hamann KJ, Pease LR, Gleich GJ. (1989). Eosinophil cationic protein cDNA. Comparison with other toxic cationic proteins and ribonucleases. J Immunol, 143, 952–955.
  • Bedoya VI, Boasso A, Hardy AW, Rybak S, Shearer GM, Rugeles MT. (2006). Ribonucleases in HIV type 1 inhibition: effect of recombinant RNases on infection of primary T cells and immune activation-induced RNase gene and protein expression. AIDS Res Hum Retroviruses, 22, 897–907.
  • Blanchard C, Rothenberg ME. (2009). Biology of the eosinophil. Adv Immunol, 101, 81–121.
  • Boix E, Leonidas DD, Nikolovski Z, Nogués MV, Cuchillo CM, Acharya KR. (1999). Crystal structure of eosinophil cationic protein at 2.4 A resolution. Biochemistry, 38, 16794–16801.
  • Bolscher BG, Plat H, Wever R. (1984). Some properties of human eosinophil peroxidase, a comparison with other peroxidases. Biochim Biophys Acta, 784, 177–186.
  • Bonno M, Kephart GM, Carlson CM, Loegering DA, Vernof KK, Gleich GJ. (1994). Expression of eosinophil-granule major basic protein messenger ribonucleic acid in placental X cells. Lab Invest, 70, 234–241.
  • Borelli V, Vita F, Shankar S, Soranzo MR, Banfi E, Scialino G, Brochetta C, Zabucchi G. (2003). Human eosinophil peroxidase induces surface alteration, killing, and lysis of Mycobacterium tuberculosis. Infect Immun, 71, 605–613.
  • Bousquet J, Chanez P, Lacoste JY, Barnéon G, Ghavanian N, Enander I, Venge P, Ahlstedt S, Simony-Lafontaine J, Godard P. (1990). Eosinophilic inflammation in asthma. N Engl J Med, 323, 1033–1039.
  • Burke GJ. (1975). Investigations on the level of circulating eosinophils throughout a 24 hour period in parasitic disease. Trans R Soc Trop Med Hyg, 69, 402–405.
  • Busse WW, Lemanske RF Jr. (2001). Asthma. N Engl J Med, 344, 350–362.
  • Butterworth AE. (1977). The eosinophil and its role in immunity to helminth infection. Curr Top Microbiol Immunol, 77, 127–168.
  • Butterworth AE. (1984). Cell-mediated damage to helminths. Adv Parasitol, 23, 143–235.
  • Butterworth AE, Sturrock RF, Houba V, Mahmoud AA, Sher A, Rees PH. (1975). Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature, 256, 727–729.
  • Butterworth AE, David JR, Franks D, Mahmoud AA, David PH, Sturrock RF, Houba V. (1977). Antibody-dependent eosinophil-mediated damage to 51Cr-labeled schistosomula of Schistosoma mansoni: damage by purieid eosinophils. J Exp Med, 145, 136–150.
  • Butterworth AE, Wassom DL, Gleich GJ, Loegering DA, David JR. (1979). Damage to schistosomula of Schistosoma mansoni induced directly by eosinophil major basic protein. J Immunol, 122, 221–229.
  • Buys J, Wever R, Ruitenberg EJ. (1984). Myeloperoxidase is more efficient than eosinophil peroxidase in the in vitro killing of newborn larvae of Trichinella spiralis. Immunology, 51, 601–607.
  • Capron M, Kazatchkine MD, Fischer E, Joseph M, Butterworth AE, Kusnierz JP, Prin L, Papin JP, Capron A. (1987). Functional role of the α-chain of complement receptor type 3 in human eosinophil-dependent antibody-mediated cytotoxicity against schistosomes. J Immunol, 139, 2059–2065.
  • Cara A, Rybak SM, Newton DL, Crowley R, Rottschafer SE, Reitz MS Jr, Gusella GL. (1998). Inhibition of HIV-1 replication by combined expression of gag dominant negative mutant and a human ribonuclease in a tightly controlled HIV-1 inducible vector. Gene Ther, 5, 65–75.
  • Carlson MG, Peterson CG, Venge P. (1985). Human eosinophil peroxidase: purification and characterization. J Immunol, 134, 1875–1879.
  • Carreras E, Boix E, Rosenberg HF, Cuchillo CM, Nogués MV. (2003). Both aromatic and cationic residues contribute to the membrane-lytic and bactericidal activity of eosinophil cationic protein. Biochemistry, 42, 6636–6644.
  • Carreras E, Boix E, Navarro S, Rosenberg HF, Cuchillo CM, Nogués MV. (2005). Surface-exposed amino acids of eosinophil cationic protein play a critical role in the inhibition of mammalian cell proliferation. Mol Cell Biochem, 272, 1–7.
  • Chang KC, Lo CW, Fan TC, Chang MD, Shu CW, Chang CH, Chung CT, Fang SL, Chao CC, Tsai JJ, Lai YK. (2010). TNF-α mediates eosinophil cationic protein-induced apoptosis in BEAS-2B cells. BMC Cell Biol, 11, 6.
  • Clegg JA, Smithers SR, Terry RJ. (1971). Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature, 232, 653–654.
  • Collins PD, Marleau S, Griffiths-Johnson DA, Jose PJ, Williams TJ. (1995). Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med, 182, 1169–1174.
  • Colocho Zelaya EA, Orvell C, Strannegård O. (1994). Eosinophil cationic protein in nasopharyngeal secretions and serum of infants infected with respiratory syncytial virus. Pediatr Allergy Immunol, 5, 100–106.
  • Davis MD, Plager DA, George TJ, Weiss EA, Gleich GJ, Leiferman KM. (2003). Interactions of eosinophil granule proteins with skin: limits of detection, persistence, and vasopermeabilization. J Allergy Clin Immunol, 112, 988–994.
  • Davoine F, Cao M, Wu Y, Ajamian F, Ilarraza R, Kokaji AI, Moqbel R, Adamko DJ. (2008). Virus-induced eosinophil mediator release requires antigen-presenting and CD4+ T cells. J Allergy Clin Immunol, 122, 69–77, 77.
  • De Monchy JG, Kauffman HF, Venge P, Koëter GH, Jansen HM, Sluiter HJ, De Vries K. (1985). Bronchoalveolar eosinophilia during allergen-induced late asthmatic reactions. Am Rev Respir Dis, 131, 373–376.
  • de Beer T, Vliegenthart JF, Löffler A, Hofsteenge J. (1995). The hexopyranosyl residue that is C-glycosidically linked to the side chain of tryptophan-7 in human RNase Us is alpha-mannopyranose. Biochemistry, 34, 11785–11789.
  • Dean DA, Wistar R, Murrell KD. (1974). Combined in vitro effects of rat antibody and neutrophilic leukocytes on schistosomula of Schistosoma mansoni. Am J Trop Med Hyg, 23, 420–428.
  • Desakorn V, Suntharasamai P, Pukrittayakamee S, Migasena S, Bunnag D. (1987). Adherence of human eosinophils to infective filariform larvae of Necator americanus in vitro. Southeast Asian J Trop Med Public Health, 18, 66–72.
  • Dessein AJ, Parker WL, James SL, David JR. (1981). IgE antibody and resistance to infection. I. Selective suppression of the IgE antibody response in rats diminishes the resistance and the eosinophil response to Trichinella spiralis infection. J Exp Med, 153, 423–436.
  • Dimayuga E, Stober M, Kayes SG. (1991). Eosinophil peroxidase levels in hearts and lungs of mice infected with Toxocara canis. J Parasitol, 77, 461–466.
  • Ding J, Liu J, Xue CF, Li YH, Gong WD. (2003). Construction and expression of prokaryotic expression vector for pTAT-HBV targeted ribonuclease fusion protein. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi, 19, 49–51.
  • Domachowske JB, Rosenberg HF. (1997). Eosinophils inhibit retroviral transduction of human target cells by a ribonuclease-dependent mechanism. J Leukoc Biol, 62, 363–368.
  • Domachowske JB, Dyer KD, Bonville CA, Rosenberg HF. (1998a). Recombinant human eosinophil-derived neurotoxin/RNase 2 functions as an effective antiviral agent against respiratory syncytial virus. J Infect Dis, 177, 1458–1464.
  • Domachowske JB, Bonville CA, Dyer KD, Rosenberg HF. (1998b). Evolution of antiviral activity in the ribonuclease A gene superfamily: evidence for a specific interaction between eosinophil-derived neurotoxin (EDN/RNase 2) and respiratory syncytial virus. Nucleic Acids Res, 26, 5327–5332.
  • Domachowske JB, Dyer KD, Adams AG, Leto TL, Rosenberg HF. (1998c). Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res, 26, 3358–3363.
  • Durack DT, Sumi SM, Klebanoff SJ. (1979). Neurotoxicity of human eosinophils. Proc Natl Acad Sci USA, 76, 1443–1447.
  • Durack DT, Ackerman SJ, Loegering DA, Gleich GJ. (1981). Purification of human eosinophil-derived neurotoxin. Proc Natl Acad Sci USA, 78, 5165–5169.
  • Dvorak AM, Ackerman SJ, Furitsu T, Estrella P, Letourneau L, Ishizaka T. (1992). Mature eosinophils stimulated to develop in human-cord blood mononuclear cell cultures supplemented with recombinant human interleukin-5. II. Vesicular transport of specific granule matrix peroxidase, a mechanism for effecting piecemeal degranulation. Am J Pathol, 140, 795–807.
  • Dziarski R, Gupta D. (2005). Peptidoglycan recognition in innate immunity. J Endotoxin Res, 11, 304–310.
  • Elsbach P, Weiss J, Levy O. (1999). Oxygen-independent antimicrobial systems of phagocytes. In: Gallin, JI, Snyderman, R, Fearon, DT, Haynes, BF, Nathan, C. eds, Inflammation: Basic Principles and Clinical Correlates. Baltimore, Md: Lippincott Williams and Wilkins Co., pp 801–817.
  • Eriksson J, Woschnagg C, Fernvik E, Venge P. (2007). A SELDI-TOF MS study of the genetic and post-translational molecular heterogeneity of eosinophil cationic protein. J Leukoc Biol, 82, 1491–1500.
  • Fan TC, Chang HT, Chen IW, Wang HY, Chang MD. (2007). A heparan sulfate-facilitated and raft-dependent macropinocytosis of eosinophil cationic protein. Traffic, 8, 1778–1795.
  • Fan TC, Fang SL, Hwang CS, Hsu CY, Lu XA, Hung SC, Lin SC, Chang MD. (2008). Characterization of molecular interactions between eosinophil cationic protein and heparin. J Biol Chem, 283, 25468–25474.
  • Frigas E, Loegering DA, Gleich GJ. (1980). Cytotoxic effects of the guinea pig eosinophil major basic protein on tracheal epithelium. Lab Invest, 42, 35–43.
  • Furuta GT, Nieuwenhuis EE, Karhausen J, Gleich G, Blumberg RS, Lee JJ, Ackerman SJ. (2005). Eosinophils alter colonic epithelial barrier function: role for major basic protein. Am J Physiol Gastrointest Liver Physiol, 289, G890–G897.
  • Futami J, Tsushima Y, Murato Y, Tada H, Sasaki J, Seno M, Yamada H. (1997). Tissue-specific expression of pancreatic-type RNases and RNase inhibitor in humans. DNA Cell Biol, 16, 413–419.
  • Gandhi NS, Mancera RL. (2008). The structure of glycosaminoglycans and their interactions with proteins. Chem Biol Drug Des, 72, 455–482.
  • Ganem D, Varmus HE. (1987). The molecular biology of the hepatitis B viruses. Annu Rev Biochem, 56, 651–693.
  • Garofalo R, Kimpen JL, Welliver RC, Ogra PL. (1992). Eosinophil degranulation in the respiratory tract during naturally acquired respiratory syncytial virus infection. J Pediatr, 120, 28–32.
  • Glauert AM, Butterworth AE, Sturrock RF, Houba V. (1978). The mechansim of antibody-dependent, eosinophil-mediated damage to schistosomula of Schistosoma mansoni in vitro: a study by phase-contrast and electron microscopy. J Cell Sci, 34, 173–192.
  • Gleich GJ. (1989). Eosinophils, basophils, and mast cells. J Allergy Clin Immunol, 84, 1024–1027.
  • Gleich GJ, Adolphson CR. (1986). The eosinophilic leukocyte: structure and function. Adv Immunol, 39, 177–253.
  • Gleich GJ, Loegering DA. (1984). Immunobiology of eosinophils. Annu Rev Immunol, 2, 429–459.
  • Gleich GJ, Loegering DA, Bell MP, Checkel JL, Ackerman SJ, McKean DJ. (1986). Biochemical and functional similarities between human eosinophil-derived neurotoxin and eosinophil cationic protein: homology with ribonuclease. Proc Natl Acad Sci USA, 83, 3146–3150.
  • Gleich GJ, Adolphson CR, Leiferman KM. (1993). The biology of the eosinophilic leukocyte. Annu Rev Med, 44, 85–101.
  • Goetzl EJ. (1982). The conversion of leukotriene C4 to isomers of leukotriene B4 by human eosinophil peroxidase. Biochem Biophys Res Commun, 106, 270–275.
  • Goldring OL, Clegg JA, Smithers SR, Terry RJ. (1976). Acquisition of human blood group antigens by Schistosoma mansoni. Clin Exp Immunol, 26, 181–187.
  • Gong WD, Liu J, Ding J, Zhao Y, Li YH, Xue CF. (2003). Inhibition of HBV targeted ribonuclease enhanced by introduction of linker. World J Gastroenterol, 9, 1504–1507.
  • Gordon MH. (1933). Remarks on Hodgkin’s disease, a pathogenic agent in the glands, and its application in diagnosis. Br Med J, 1, 641–644.
  • Hamann KJ, Barker RL, Loegering DA, Gleich GJ. (1987). Comparative toxicity of purified human eosinophil granule proteins for newborn larvae of Trichinella spiralis. J Parasitol, 73, 523–529.
  • Hamann KJ, Ten RM, Loegering DA, Jenkins RB, Heise MT, Schad CR, Pease LR, Gleich GJ, Barker RL. (1990a). 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.
  • Hamann KJ, Gleich GJ, Checkel JL, Loegering DA, McCall JW, Barker RL. (1990b). In vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. J Immunol, 144, 3166–3173.
  • Hamann KJ, Barker RL, Ten RM, Gleich GJ. (1991). The molecular biology of eosinophil granule proteins. Int Arch Allergy Appl Immunol, 94, 202–209.
  • Hassan MM, el-Motaim MH, Mattar MA, Afify HA, el-Badrawy el-S. (2002). Assessing the morbidity of schistosomiasis by measuring eosinophil cationic protein in serum. J Egypt Soc Parasitol, 32, 517–524.
  • Henderson WR, Chi EY, Klebanoff SJ. (1980). Eosinophil peroxidase-induced mast cell secretion. J Exp Med, 152, 265–279.
  • Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. (1998). Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays, 20, 156–167.
  • Hisamatsu K, Ganbo T, Nakazawa T, Murakami Y, Gleich GJ, Makiyama K, Koyama H. (1990). Cytotoxicity of human eosinophil granule major basic protein to human nasal sinus mucosa in vitro. J Allergy Clin Immunol, 86, 52–63.
  • Hsü SY, Lust GL, Hsü HF. (1971). The fate of challenge schistosome cercariae in a monkey immunized by cercariae exposed to high doses of x-irradiation. Proc Soc Exp Biol Med, 136, 727–731.
  • Jong EC, Chi EY, Klebanoff SJ. (1984). Human neutrophil-mediated killing of schistosomula of Schistosoma mansoni: augmentation by schistosomal binding of eosinophil peroxidase. Am J Trop Med Hyg, 33, 104–115.
  • Jong EC, Mahmoud AA, Klebanoff SJ. (1981). Peroxidase-mediated toxicity to schistosomula of Schistosoma mansoni. J Immunol, 126, 468–471.
  • Jönsson UB, Byström J, Stålenheim G, Venge P. (2002). Polymorphism of the eosinophil cationic protein-gene is related to the expression of allergic symptoms. Clin Exp Allergy, 32, 1092–1095.
  • Kay AB. (1985). Eosinophils as effector cells in immunity and hypersensitivity disorders. Clin Exp Immunol, 62, 1–12.
  • Kazura JW, Fanning MM, Blumer JL, Mahmoud AA. (1981). Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula of Schistosoma mansoni in vitro. J Clin Invest, 67, 93–102.
  • Kephart GM, Gleich GJ, Connor DH, Gibson DW, Ackerman SJ. (1984). Deposition of eosinophil granule major basic protein onto microfilariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Lab Invest, 50, 51–61.
  • Kephart GM, Andrade ZA, Gleich GJ. (1988). Localization of eosinophil major basic protein onto eggs of Schistosoma mansoni in human pathologic tissue. Am J Pathol, 133, 389–396.
  • Kierszenbaum F, Villalta F, Tai PC. (1986). Role of inflammatory cells in Chagas’ disease. III. Kinetics of human eosinophil activation upon interaction with parasites (Trypanosoma cruzi). J Immunol, 136, 662–666.
  • Kita H. (1996). The eosinophil: a cytokine-producing cell? J Allergy Clin Immunol, 97, 889–892.
  • Klebanoff SJ. (1999). Oxygen metabolites from phagocytes. Baltimore, MD: Lippincott Williams and Wilkins Co., pp 721–768.
  • Klion AD, Nutman TB. (2004). The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol, 113, 30–37.
  • Krieg J, Gläsner W, Vicentini A, Doucey MA, Löffler A, Hess D, Hofsteenge J. (1997). C-Mannosylation of human RNase 2 is an intracellular process performed by a variety of cultured cells. J Biol Chem, 272, 26687–26692.
  • Lee NA, Gelfand EW, Lee JJ. (2001). Pulmonary T cells and eosinophils: coconspirators or independent triggers of allergic respiratory pathology? J Allergy Clin Immunol, 107, 945–957.
  • Lehrer RI, Szklarek D, Barton A, Ganz T, Hamann KJ, Gleich GJ. (1989). Antibacterial properties of eosinophil major basic protein and eosinophil cationic protein. J Immunol, 142, 4428–4434.
  • Li YH, Liu, J., Xue, C.F. (2002). Construction of HBV targeted ribonuclease and its expression in 2.2.15 cell line. Xibao yu Fenzi Mianyixue Zazhi, 18, 217.
  • Li Y, Zhao Y, Liu J, Huang Y, Liu Z, Xue C. (2010). A promising alternative anti-HBV agent: the targeted ribonuclease. Int J Mol Med, 26, 51–56.
  • Liu J, Li YH, Xue CF, Ding J, Gong WD, Zhao Y, Huang YX. (2003). Targeted ribonuclease can inhibit replication of hepatitis B virus. World J Gastroenterol, 9, 295–299.
  • Mackenzie CD, Jungery M, Taylor PM, Ogilvie BM. (1981). The in-vitro interaction of eosinophils, neutrophils, macrophages and mast cells with nematode surfaces in the presence of complement or antibodies. J Pathol, 133, 161–175.
  • MacPherson JC, Comhair SA, Erzurum SC, Klein DF, Lipscomb MF, Kavuru MS, Samoszuk MK, Hazen SL. (2001). Eosinophils are a major source of nitric oxide-derived oxidants in severe asthma: characterization of pathways available to eosinophils for generating reactive nitrogen species. J Immunol, 166, 5763–5772.
  • Maddox DE, Kephart GM, Coulam CB, Butterfield JH, Benirschke K, Gleich GJ. (1984). Localization of a molecule immunochemically similar to eosinophil major basic protein in human placenta. J Exp Med, 160, 29–41.
  • Magnaval JF, Berry A, Fabre R, Morassin B. (2001). Eosinophil cationic protein as a possible marker of active human Toxocara infection. Allergy, 56, 1096–1099.
  • Magnaval JF, Faufingue JH, Morassin B, Fabre R. (2006). Eosinophil cationic protein, specific IgE and IgG4 in human toxocariasis. J Helminthol, 80, 417–423.
  • Mahmoud AA, Warren KS, Peters PA. (1975). A role for the eosinophil in acquired resistance to Schistosoma mansoni infection as determined by antieosinophil serum. J Exp Med, 142, 805–813.
  • Maizels RM, Yazdanbakhsh M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol, 3, 733–744.
  • Mayeno AN, Curran AJ, Roberts RL, Foote CS. (1989). Eosinophils preferentially use bromide to generate halogenating agents. J Biol Chem, 264, 5660–5668.
  • McCormick ML, Roeder TL, Railsback MA, Britigan BE. (1994). Eosinophil peroxidase-dependent hydroxyl radical generation by human eosinophils. J Biol Chem, 269, 27914–27919.
  • McGrogan M, Simonsen C, Scott R, Griffith J, Ellis N, Kennedy J, Campanelli D, Nathan C, Gabay J. (1988). Isolation of a complementary DNA clone encoding a precursor to human eosinophil major basic protein. J Exp Med, 168, 2295–2308.
  • McLaren DJ, McKean JR, Olsson I, Venges P, Kay AB. (1981). Morphological studies on the killing of schistosomula of Schistosoma mansoni by human eosinophil and neutrophil cationic proteins in vitro. Parasite Immunol, 3, 359–373.
  • McLaren DJ, Peterson CG, Venge P. (1984). Schistosoma manson: further studies of the interaction between schistosomula and granulocyte-derived cationic proteins in vitro. Parasitology, 88 (Pt 3), 491–503.
  • Meeusen EN, Balic A. (2000). Do eosinophils have a role in the killing of helminth parasites? Parasitol Today (Regul Ed), 16, 95–101.
  • Mehlhorn H, Becker B, Andrews P, Thomas H, Frenkel JK. (1981). In vivo and in vitro experiments on the effects of praziquantel on Schistosoma mansoni.A light and electron microscopic study. Arzneimittelforschung, 31, 544–554.
  • Metcalf D, Burgess AW, Johnson GR, Nicola NA, Nice EC, DeLamarter J, Thatcher DR, Mermod JJ. (1986). In vitro actions on hemopoietic cells of recombinant murine GM-CSF purified after production in Escherichia coli: comparison with purified native GM-CSF. J Cell Physiol, 128, 421–431.
  • Metcalf D, Begley CG, Nicola NA, Johnson GR. (1987). Quantitative responsiveness of murine hemopoietic populations in vitro and in vivo to recombinant multi-CSF (IL-3). Exp Hematol, 15, 288–295.
  • Migler R, DeChatelet LR, Bass DA. (1978). Human eosinophilic peroxidase: role in bactericidal activity. Blood, 51, 445–456.
  • Milbourne EA, Howell MJ. (1993). Eosinophil differentiation in response to Fasciola hepatica and its excretory/secretory antigens. Int J Parasitol, 23, 1005–1009.
  • Molina HA, Kierszenbaum F, Hamann KJ, Gleich GJ. (1988). Toxic effects produced or mediated by human eosinophil granule components on Trypanosoma cruzi. Am J Trop Med Hyg, 38, 327–334.
  • Monteseirín J, Vega A, Chacón P, Camacho MJ, El Bekay R, Asturias JA, Martínez A, Guardia P, Pérez-Cano R, Conde J. (2007). Neutrophils as a novel source of eosinophil cationic protein in IgE-mediated processes. J Immunol, 179, 2634–2641.
  • Motojima S, Frigas E, Loegering DA, Gleich GJ. (1989). Toxicity of eosinophil cationic proteins for guinea pig tracheal epithelium in vitro. Am Rev Respir Dis, 139, 801–805.
  • Natsoulis G, Boeke JD. (1991). New antiviral strategy using capsid-nuclease fusion proteins. Nature, 352, 632–635.
  • Navarro S, Boix E, Cuchillo CM, Nogués MV. (2010). Eosinophil-induced neurotoxicity: the role of eosinophil cationic protein/RNase 3. J Neuroimmunol, 227, 60–70.
  • O’Donnell MC, Ackerman SJ, Gleich GJ, Thomas LL. (1983). Activation of basophil and mast cell histamine release by eosinophil granule major basic protein. J Exp Med, 157, 1981–1991.
  • Paul CC, Ackerman SJ, Mahrer S, Tolbert M, Dvorak AM, Baumann MA. (1994). Cytokine induction of granule protein synthesis in an eosinophil-inducible human myeloid cell line, AML14. J Leukoc Biol, 56, 74–79.
  • Pearson RD, Uydess IL, Chapman SW, Steigbigel RT. (1987). Interaction of human eosinophils with Leishmania donovani. Ann Trop Med Parasitol, 81, 735–739.
  • Persson T, Andersson P, Bodelsson M, Laurell M, Malm J, Egesten A. (2001). Bactericidal activity of human eosinophilic granulocytes against Escherichia coli. Infect Immun, 69, 3591–3596.
  • Peters MS, Rodriguez M, Gleich GJ. (1986). Localization of human eosinophil granule major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin by immunoelectron microscopy. Lab Invest, 54, 656–662.
  • Peterson CG, Jörnvall H, Venge P. (1988). Purification and characterization of eosinophil cationic protein from normal human eosinophils. Eur J Haematol, 40, 415–423.
  • Phipps S, Lam CE, Mahalingam S, Newhouse M, Ramirez R, Rosenberg HF, Foster PS, Matthaei KI. (2007). Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood, 110, 1578–1586.
  • Pincus SH, Butterworth AE, David JR, Robbins M, Vadas MA. (1981). Antibody-dependent eosinophil-mediated damage to schistosomula of Schistosoma mansoni: lack of requirement for oxidative metabolism. J Immunol, 126, 1794–1799.
  • Pinto LA, Sharpe S, Cohen DI, Shearer GM. (1998). Alloantigen-stimulated anti-HIV activity. Blood, 92, 3346–3354.
  • Pinto LA, Blazevic V, Shearer GM, Patterson BK, Dolan MJ. (2000). Alloantigen-induced anti-HIV activity occurs prior to reverse transcription and can be generated by leukocytes from HIV-infected individuals. Blood, 95, 1875–1876.
  • Plager DA, Loegering DA, Checkel JL, Tang J, Kephart GM, Caffes PL, Adolphson CR, Ohnuki LE, Gleich GJ. (2006). Major basic protein homolog (MBP2): a specific human eosinophil marker. J Immunol, 177, 7340–7345.
  • Popken-Harris P, Checkel J, Loegering D, Madden B, Springett M, Kephart G, Gleich GJ. (1998). Regulation and processing of a precursor form of eosinophil granule major basic protein (ProMBP) in differentiating eosinophils. Blood, 92, 623–631.
  • Qadri F, Bhuiyan TR, Dutta KK, Raqib R, Alam MS, Alam NH, Svennerholm AM, Mathan MM. (2004). Acute dehydrating disease caused by Vibrio cholerae serogroups O1 and O139 induce increases in innate cells and inflammatory mediators at the mucosal surface of the gut. Gut, 53, 62–69.
  • Ramos AL, Discipio RG, Ferreira AM. (2006). Eosinophil cationic protein damages protoscoleces in vitro and is present in the hydatid cyst. Parasite Immunol, 28, 347–355.
  • Raqib R, Moly PK, Sarker P, Qadri F, Alam NH, Mathan M, Andersson J. (2003). Persistence of mucosal mast cells and eosinophils in Shigella-infected children. Infect Immun, 71, 2684–2692.
  • Rosenberg HF. (1995). Recombinant human eosinophil cationic protein. Ribonuclease activity is not essential for cytotoxicity. J Biol Chem, 270, 7876–7881.
  • Rosenberg HF. (1999). The eosinophil. In: Gallin, JI, Snyderman, R, Fearon, DT, Haynes, BF, Nathan, C. eds, Inflammation: Basic Principles and Clinical Correlates. Baltimore, Md: Lippincott Williams and Wilkins Co., pp. 61–77.
  • Rosenberg HF, Domachowske JB. (2001). Eosinophils, eosinophil ribonucleases, and their role in host defense against respiratory virus pathogens. J Leukoc Biol, 70, 691–698.
  • Rosenberg HF, Tenen DG, Ackerman SJ. (1989a). Molecular cloning of the human eosinophil-derived neurotoxin: a member of the ribonuclease gene family. Proc Natl Acad Sci USA, 86, 4460–4464.
  • Rosenberg HF, Ackerman SJ, Tenen DG. (1989b). Human eosinophil cationic protein. Molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. J Exp Med, 170, 163–176.
  • Rosenberg HF, Dyer KD, Domachowske JB. (2009). Eosinophils and their interactions with respiratory virus pathogens. Immunol Res, 43, 128–137.
  • Rothenberg ME. (1998). Eosinophilia. N Engl J Med, 338, 1592–1600.
  • Rugeles MT, Trubey CM, Bedoya VI, Pinto LA, Oppenheim JJ, Rybak SM, Shearer GM. (2003). Ribonuclease is partly responsible for the HIV-1 inhibitory effect activated by HLA alloantigen recognition. AIDS, 17, 481–486.
  • Saito S, Hamada A, Watanabe N, Obata T, Katakura K, Ohtomo H. (1996). Eosinophil chemotactic activity in Leishmania amazonensis promastigotes. Parasitol Res, 82, 485–489.
  • Sakamaki K, Tomonaga M, Tsukui K, Nagata S. (1989). Molecular cloning and characterization of a chromosomal gene for human eosinophil peroxidase. J Biol Chem, 264, 16828–16836.
  • Sánchez D, Moussaoui M, Carreras E, Torrent M, Nogués V, Boix E. (2011). Mapping the eosinophil cationic protein antimicrobial activity by chemical and enzymatic cleavage. Biochimie, 93, 331–338.
  • Sanderson CJ. (1992). Interleukin-5, eosinophils, and disease. Blood, 79, 3101–3109.
  • Sher A, Hall BF, Vadas MA. (1978). Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. J Exp Med, 148, 46–57.
  • Shi HZ. (2004). Eosinophils function as antigen-presenting cells. J Leukoc Biol, 76, 520–527.
  • Sigurs N, Bjarnason R, Sigurbergsson F. (1994). Eosinophil cationic protein in nasal secretion and in serum and myeloperoxidase in serum in respiratory syncytial virus bronchiolitis: relation to asthma and atopy. Acta Paediatr, 83, 1151–1155.
  • Silberstein DS, David JR. (1986). Tumor necrosis factor enhances eosinophil toxicity to Schistosoma mansoni larvae. Proc Natl Acad Sci USA, 83, 1055–1059.
  • Singh A, Batra JK. (2011). Role of unique basic residues in cytotoxic, antibacterial and antiparasitic activities of human eosinophil cationic protein. Biol Chem, 392, 337–346.
  • Svensson L, Wennerås C. (2005). Human eosinophils selectively recognize and become activated by bacteria belonging to different taxonomic groups. Microbes Infect, 7, 720–728.
  • Swaminathan GJ, Weaver AJ, Loegering DA, Checkel JL, Leonidas DD, Gleich GJ, Acharya KR. (2001). Crystal structure of the eosinophil major basic protein at 1.8 A. An atypical lectin with a paradigm shift in specificity. J Biol Chem, 276, 26197–26203.
  • Swaminathan GJ, Holloway DE, Veluraja K, Acharya KR. (2002). Atomic resolution (0.98 A) structure of eosinophil-derived neurotoxin. Biochemistry, 41, 3341–3352.
  • Swaminathan GJ, Myszka DG, Katsamba PS, Ohnuki LE, Gleich GJ, Acharya KR. (2005). Eosinophil-granule major basic protein, a C-type lectin, binds heparin. Biochemistry, 44, 14152–14158.
  • Tarleton RL, Kemp WM. (1981). Demonstration of IgG-Fc and C3 receptors on adult Schistosoma mansoni. J Immunol, 126, 379–384.
  • Ten RM, Pease LR, McKean DJ, Bell MP, Gleich GJ. (1989). Molecular cloning of the human eosinophil peroxidase. Evidence for the existence of a peroxidase multigene family. J Exp Med, 169, 1757–1769.
  • Tiffany HL, Li F, Rosenberg HF. (1995). Hyperglycosylation of eosinophil ribonucleases in a promyelocytic leukemia cell line and in differentiated peripheral blood progenitor cells. J Leukoc Biol, 58, 49–54.
  • Tischendorf FW, Brattig NW, Büttner DW, Pieper A, Lintzel M. (1996). Serum levels of eosinophil cationic protein, eosinophil-derived neurotoxin and myeloperoxidase in infections with filariae and schistosomes. Acta Trop, 62, 171–182.
  • Torrent M, Cuyás E, Carreras E, Navarro S, López O, de la Maza A, Nogués MV, Reshetnyak YK, Boix E. (2007). Topography studies on the membrane interaction mechanism of the eosinophil cationic protein. Biochemistry, 46, 720–733.
  • Torrent M, Navarro S, Moussaoui M, Nogués MV, Boix E. (2008). Eosinophil cationic protein high-affinity binding to bacteria-wall lipopolysaccharides and peptidoglycans. Biochemistry, 47, 3544–3555.
  • Torrent M, Nogués VM, Boix E. (2009a). A theoretical approach to spot active regions in antimicrobial proteins. BMC Bioinformatics, 10, 373.
  • Torrent M, Sánchez D, Buzón V, Nogués MV, Cladera J, Boix E. (2009b). Comparison of the membrane interaction mechanism of two antimicrobial RNases: RNase 3/ECP and RNase 7. Biochim Biophys Acta, 1788, 1116–1125.
  • Torrent M, Odorizzi F, Nogués MV, Boix E. (2010a). Eosinophil cationic protein aggregation: identification of an N-terminus amyloid prone region. Biomacromolecules, 11, 1983–1990.
  • Torrent M, Badia M, Moussaoui M, Sanchez D, Nogués MV, Boix E. (2010b). Comparison of human RNase 3 and RNase 7 bactericidal action at the Gram-negative and Gram-positive bacterial cell wall. FEBS J, 277, 1713–1725.
  • Torrent M, Nogués MV, Boix E. (2011). Eosinophil cationic protein (ECP) can bind heparin and other glycosaminoglycans through its RNase active site. J Mol Recognit, 24, 90–100.
  • Trulson A, Byström J, Engström A, Larsson R, 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.
  • Ulrich M, Petre A, Youhnovski N, Prömm F, Schirle M, Schumm M, Pero RS, Doyle A, Checkel J, Kita H, Thiyagarajan N, Acharya KR, Schmid-Grendelmeier P, Simon HU, Schwarz H, Tsutsui M, Shimokawa H, Bellon G, Lee JJ, Przybylski M, Döring G. (2008). Post-translational tyrosine nitration of eosinophil granule toxins mediated by eosinophil peroxidase. J Biol Chem, 283, 28629–28640.
  • Venge P, Byström J, Carlson M, Hâkansson L, Karawacjzyk M, Peterson C, Sevéus L, Trulson A. (1999). Eosinophil cationic protein (ECP): molecular and biological properties and the use of ECP as a marker of eosinophil activation in disease. Clin Exp Allergy, 29, 1172–1186.
  • Villalta F, Kierszenbaum F. (1984). Role of inflammatory cells in Chagas’ disease. I. Uptake and mechanism of destruction of intracellular (amastigote) forms of Trypanosoma cruzi by human eosinophils. J Immunol, 132, 2053–2058.
  • Villalta F, Pankratz HS, Kierszenbaum F. (1987). Extracellular killing of Trypanosoma cruzi amastigotes by human eosinophils. J Protozool, 34, 285–290.
  • Voehringer D, van Rooijen N, Locksley RM. (2007). Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J Leukoc Biol, 81, 1434–1444.
  • Wardlaw AJ, Brightling C, Green R, Woltmann G, Pavord I. (2000). Eosinophils in asthma and other allergic diseases. Br Med Bull, 56, 985–1003.
  • Waters LS, Taverne J, Tai PC, Spry CJ, Targett GA, Playfair JH. (1987). Killing of Plasmodium falciparum by eosinophil secretory products. Infect Immun, 55, 877–881.
  • Weller PF. (1994). Eosinophils: structure and functions. Curr Opin Immunol, 6, 85–90.
  • Winqvist I, Olofsson T, Persson E. (1985). Effect of zinc and other cations on the release of the eosinophil cationic protein. Scand J Clin Lab Invest, 45, 671–677.
  • Wintrobe MM. (1961). Clinical Hematology. Philadelphia: Lea & Febiger.
  • Woschnagg C, Rubin J, Venge P. (2009). Eosinophil cationic protein (ECP) is processed during secretion. J Immunol, 183, 3949–3954.
  • Wu CM, Chang MD. (2004). Signal peptide of eosinophil cationic protein is toxic to cells lacking signal peptide peptidase. Biochem Biophys Res Commun, 322, 585–592.
  • Wu W, Chen Y, Hazen SL. (1999). Eosinophil peroxidase nitrates protein tyrosyl residues. Implications for oxidative damage by nitrating intermediates in eosinophilic inflammatory disorders. J Biol Chem, 274, 25933–25944.
  • Yamaguchi Y, Suda T, Suda J, Eguchi M, Miura Y, Harada N, Tominaga A, Takatsu K. (1988). Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J Exp Med, 167, 43–56.
  • Yazdanbakhsh M, Tai PC, Spry CJ, Gleich GJ, Roos D. (1987). Synergism between eosinophil cationic protein and oxygen metabolites in killing of schistosomula of Schistosoma mansoni. J Immunol, 138, 3443–3447.
  • Yoon J, Ponikau JU, Lawrence CB, Kita H.. (2008). Innate antifungal immunity of human eosinophils mediated by a β 2 integrin. CD11b. J Immunol, 181, 2907–2915.
  • Young JD, Peterson CG, Venge P, Cohn ZA. (1986). Mechanism of membrane damage mediated by human eosinophil cationic protein. Nature, 321, 613–616.
  • Young B, Lowe, JS, Stevens A, Heath JW. (2006). Wheater’s functional histology, a text and colour atlas. Edinburgh: Elsevier Churchill Livingstone.
  • Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU. (2008). Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med, 14, 949–953.
  • Zhang J, Rosenberg HF. (2000). Sequence variation at two eosinophil-associated ribonuclease loci in humans. Genetics, 156, 1949–1958.
  • Zhao Y, Li Y, Liu J, Liu Z, Huang Y, Lei J, Li S, Xue C. (2008). Adenoviral-vector mediated transfer of HBV-targeted ribonuclease can inhibit HBV replication in vivo. Biochem Biophys Res Commun, 371, 541–545.

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