Excretory-secretory products from Fasciola hepatica induce eosinophil apoptosis by a caspase-dependent mechanism

Veterinary Immunology and Immunopathology

Volumn 117, Issue 3-4, 2007, Pages 197-208

  Serradell, Marianela C ^a   Guasconi, Lorena ^a   Cervi, Laura ^a   Chiapello, Laura S ^a   Masih, Diana T ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Apoptosis; Eosinophil; Excretory secretory products; Fasciola hepatica; Immunoevasion

Indexed keywords

ANTIGEN; CARBOHYDRATE DERIVATIVE; CASPASE; GENISTEIN; INTERLEUKIN 12; NITRIC OXIDE; PROTEIN TYROSINE KINASE; STAUROSPORINE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EOSINOPHIL; EXCRETION; FASCIOLA HEPATICA; FASCIOLIASIS; HELMINTH; HOST RESISTANCE; IMMUNE RESPONSE; LIVER; MALE; NONHUMAN; PERITONEUM; PROTEIN SECRETION; RAT; SECRETION;

ANIMALS; ANTIGENS, HELMINTH; APOPTOSIS; CASPASES; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; EOSINOPHILS; FASCIOLA HEPATICA; FASCIOLIASIS; MICROSCOPY, ELECTRON, TRANSMISSION; PROTEIN-TYROSINE KINASES; RATS;

FASCIOLA HEPATICA; RATTUS; VERMES;

EID: 34248190295     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2007.03.007     Document Type: Article

References (53)

1. Archer S. Measurement of nitric oxide in biological models. FASEB J. 7 (1993) 349-360
2. Becker S., Fenton M.J., and Soukup J.M. Involvement of microbial components and toll-like receptors 2 and 4 in cytokine responses to air pollution particles. Am. J. Respir. Cell Mol. Biol. 27 (2002) 611-618
3. Berro A.I., Perry G.A., and Agrawal D.K. Increased expression and activation of CD30 induce apoptosis in human blood eosinophils. J. Immunol. 173 (2004) 2174-2183
4. Butterworth A.E., Wasson D.L., Gleich G.J., Loegering D.A., and David J.R. Damage to schistosomula of Schistosoma mansoni induced directly by eosinophil major basic protein. J. Immunol. 122 (1979) 221-229
5. Carmona C., Dowd A.J., Smith A.M., and Dalton J.P. Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to newly excysted juveniles. Mol. Biochem. Parasitol. 62 (1993) 9-17
6. Cervi L., Rubinstein H., and Masih D.T. Involvement of excretion-secretion products from Fasciola hepatica inducing suppression of the cellular immune responses. Vet. Parasitol. 61 (1996) 97-111
7. Cervi L., and Masih D.T. Inhibition of spleen cell proliferative response to mitogens by excretory-secretory antigens of Fasciola hepatica. Int. J. Parasitol. 27 (1997) 573-579
8. Cervi L., Rossi G., Cejas H., and Masih D.T. Fasciola hepatica-induced immune suppression of spleen mononuclear cell proliferation: role of nitric oxide. Clin. Immunol. Immunopathol. 87 (1998) 145-154
9. Chen L., Rao K.V., He Y.X., and Ramaswamy K. Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. J. Biol. Chem. 13 (2002) 34329-34335
10. Chin A.C., Teoh D.A., Scott K.G., Medding J.B., Macnaughton W.K., and Buret A.G. Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect. Immun. 70 (2002) 3673-3680
11. Chow S.C., Brown A., and Pritchard D. The human hookworm pathogen Necator americanus induces apoptosis in T lymphocytes. Parasite Immunol. 22 (2000) 21-29
12. Davies C., and Goose J. Killing of newly excysted juveniles of Fasciola hepatica in sensitized rats. Parasite Immunol. 3 (1981) 81-96
13. Dessein A., Samuelson J.C., Butterworth A.E., Hogan M., Sherry B.A., Vadas M.A., and David J.R. Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82 (1981) 357-374
14. Diaz A., Espino A.M., Marcet R., Otero O., Torres D., Finlay C.M., and Sarracent J. Partial characterization of the epitope on excretory-secretory products of Fasciola hepatica recognized by monoclonal antibody ES78. J. Parasitol. 84 (1998) 55-61
15. Espino A.M., Marcet R., and Finlay C.M. Detection of circulating excretory-secretory antigens in human fasciolosis by enzyme-linked immunosorbent assay. J. Clin. Microbiol. 28 (1990) 2637-2640
16. Gansmuller A., Anteunis A., Venturiello S.M., Bruschi F., and Binaghi R.A. Antibody-dependent in-vitro cytotoxicity of newborn Trichinella spiralis larvae: nature of the cells involved. Parasite Immunol. 9 (1987) 281-292
17. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 (1992) 493-501
18. Hanna R.E. Fasciola hepatica: glycocalyx replacement in the juvenile as a possible mechanism for protection against host immunity. Exp. Parasitol. 50 (1980) 103-114
19. Heasman S.J., Giles K.M., Ward C., Rossi A.G., Haslett C., and Dransfield I. Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation. J. Endocrinol. 178 (2003) 29-36
20. Heffernan M., Smith A., Curtain D., McDonnell S., Ryan J., and Dalton J.P. Characterization of a cathepsin-B proteinase released by Fasciola hepatica (liver fluke). Biochem. Soc. Trans. 19 (1991) 27S
21. Hillyer G.V., Soler de Galanes M., and Battisti G. Fasciola hepatica: host responders and nonresponders to parasite glutathione S-transferase. Exp. Parasitol. 75 (1992) 176-186
22. Hirsch T., Marchetti P., Susin S.A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., and Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15 (1997) 1573-1581
23. Jefferies J.R., Turner R.J., and Barrett J. Effect of Fasciola hepatica excretory-secretory products on the metabolic burst of sheep and human neutrophils. Int. J. Parasitol. 27 (1997) 1025-1029
24. Kuroda A., Uchikawa R., Matsuda S., Yamada M., Tegoshi T., and Arizono N. Up-regulation of Fas (CD95) and induction of apoptosis in intestinal epithelial cells by nematode-derived molecules. Infect. Immun. 70 (2002) 4002-4008
25. Langley R.J., and Hillyer G.V. Detection of circulating parasite antigen in murine fasciolosis by two-site enzyme-linked immunosorbent assay. Am. J. Trop. Med. Hyg. 41 (1989) 472-478
26. Lasfer M., Davenne L., Vadrot N., Alexia C., Sadji-Ouatas Z., Bringuier A.F., Feldmann G., Pessayre D., and Reyl-Desmars F. Protein kinase PKC delta and c-Abl are required for mitochondrial apoptosis induction by genotoxic stress in the absence of p53, p73 and Fas receptor. FEBS Lett. 580 (2006) 2547-2552
27. Luder C.G., Gross U., and Lopez M.F. Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions. Trends Parasitol. 17 (2001) 480-486
28. Luttmann W., Dauer E., Schmidt S., Marx O., Hossfeld M., Matthys H., and Virchow Jr. J.C. Effects of interferon-γ and tumour necrosis factor-α on CD95/Fas ligand-mediated apoptosis in human blood eosinophils. Scand. J. Immunol. 51 (2000) 54-59
29. Mahida Y.R., Galvin A., Makh S., Hyde S., Sanfilippo L., Borriello S.P., and Sewell H.F. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect. Immun. 66 (1998) 5462-5469
30. Maizels R.M., Balic A., Gomez-Escobar N., Nair M., Taylor M.D., and Allen J.E. Helminth parasites-masters of regulation. Immunol. Rev. 201 (2004) 89-116
31. Miike S., Kurasawa K., Saito Y., and Iwamoto I. Platelet-activating factor activates mitogen-activated protein kinases through the activation of phosphatidylinositol 3-kinase and tyrosine kinase in human eosinophils. J. Leukoc. Biol. 67 (2000) 117-126
32. Min D.Y., Lee Y.A., Ryu J.S., Ahn M.H., Chung Y.B., Sim S., and Shin M.H. Caspase-3-mediated apoptosis of human eosinophils by the tissue-invanding helminth Paragonimus westermani. Int. Arch. Allergy Immunol. 133 (2004) 357-364
33. Nutku E., Zhuang Q., Soussi-Gounni A., Aris F., Mazer B.D., and Hamid Q. Functional expression of IL-12 receptor by human eosinophils: IL-12 promotes eosinophil apoptosis. J. Immunol. 167 (2001) 1039-1046
34. Nutku E., Aizawa H., Hudson S.A., and Bochner B.S. Ligation of Siglec-8: a selective mechanism for induction of human eosinophil apoptosis. Blood 101 (2003) 5014-5020
35. Nutku E., Hudson S.A., and Bochner B.S. Mechanism of Siglec-8-induced human eosinophil apoptosis: role of caspases and mitochondrial injury. Biochem. Biophys. Res. Commun. 336 (2005) 918-924
36. Pinheiro R.O., Pinto E.F., Benedito A.B., Lopes U.G., and Rossi-Bergmann B. T-cell energy induced by Leishmania amazonensis antigens is related with defective antigen presentation and apoptosis. An. Acad. Bras. Cienc. 76 (2004) 519-527
37. Rainbird M.A., Macmillan D., and Meeusen E.N. Eosinophil-mediated killing of Haemonchus contortus larvae: effect of eosinophil activation and role of antibody, complement and interleukin-5. Parasite Immunol. 20 (1998) 93-103
38. Rossi G.R., Cervi L.A., García M.M., Chiapello L.S., Sastre D.A., and Masih D.T. Involvement of nitric oxide in protecting mechanism during experimental cryptococcosis. Clin. Immunol. 90 (1999) 256-265
39. Samali A., Zhivotovsky B., Jones D., Nagata S., and Orrenius S. Apoptosis: cell death defined by caspase activation. Cell Death Differ. 6 (1999) 495-496
40. Sedgwick J.B., Shikama Y., Nagata M., Brener K., and Busse W.W. Effect of isolation protocol on eosinophil function: Percoll gradients versus immunomagnetic beads. J. Immunol. Methods 198 (1996) 15-24
41. Shin M.H. Excretory-secretory product of newly excysted metacercariae of Paragonimus westermani directly induces eosinophil apoptosis. Korean J. Parasitol. 38 (2000) 17-23
42. Shin M.H., Kita H., Park H.Y., and Seoh J.Y. Cysteine protease secreted by Paragonimus westermani attenuates effector functions of human eosinophils stimulated with immunoglobulin G. Infect. Immun. 69 (2001) 1599-1604
43. Simon H.U., Yousefi S., Dibbert B., Hebestreit H., Weber M., Branch D.R., Blaser K., Levi-Schaffer F., and Anderson G.P. Role for tyrosine phosphorylation and Lyn tyrosine kinase in Fas receptor-mediated apoptosis in eosinophils. Blood 92 (1998) 547-557
44. Simon H., and Alam R. Regulation of eosinophil apoptosis: transduction of survival and death signals. Int. Arch. Allergy Immunol. 118 (1999) 7-14
45. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., Wang H.G., Reed J.C., Nicholson D.W., Alnemri E.S., Green D.R., and Martin S.J. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144 (1999) 281-292
46. Stennicke H.R., Deveraux Q.L., Humke E.W., Reed J.C., Dixit V.M., and Salvesen G.S. Caspase-9 can be activated without proteolytic processing. J. Biol. Chem. 274 (1999) 8359-8362
47. Tato P., Fernandez A.M., Solano S., Borgonio V., Garrido E., Sepulveda J., and Molinari J.L. A cysteine protease from Taenia solium metacestodes induce apoptosis in human CD4+ T-cells. Parasitol. Res. 92 (2004) 197-204
48. van der Kleij D., and Yasdanbakhsh M. Control of inflammatory diseases by pathogens: lipids and the immune system. Eur. J. Immunol. 33 (2003) 2953-2963
49. Walsh G.M., Dewson G., Wardlaw A.J., Levi-Schaffer F., and Moqbel R. A comparative study of different methods for the assessment of apoptosis and necrosis in human eosinophils. J. Immunol. Methods 217 (1998) 153-163
50. Wei S., Marches F., Borvak J., Zou W., Channon J., White M., Radke J., Cesbron-Delauw M.F., and Curiel T.J. Toxoplasma gondii-infected human myeloid dendritic cells induce T-lymphocyte dysfunction and contact-dependent apoptosis. Infect. Immun. 70 (2002) 1750-1760
51. Wong C.K., Zhang J., Ip W.K., and Lam C.W. Intracellular signal transduction in eosinophils and its clinical significance. Immunopharmacol. Immunotoxicol. 24 (2002) 165-186
52. Zhang J.P., Wong C.K., and Lam C.W. Role of caspases in dexamethasone-induced apoptosis and activation of c-Jun NH2-terminal kinase and p38 mitogen-activated protein kinase in human eosinophils. Clin. Exp. Immunol. 122 (2000) 20-27
53. Zhang X., Moilanen E., Lahti A., Hamalainen M., Giembycz M.A., Barnes P.J., Lindsay M.A., and Kankaanranta H. Regulation of eosinophil apoptosis by nitric oxide: role of c-Jun-N-terminal kinase and signal transducer and activator of transcription 5. J. Allergy Clin. Immunol. 112 (2003) 93-101