Suppression of host Th1-type granulomatous inflammation by Taenia solium metacestodes is related to down-regulation of osteopontin gene expression

International Journal for Parasitology

Volumn 38, Issue 2, 2008, Pages 239-248

  Wang, I Chuang ^a   Fan, Ping Chin ^b   Lu, Sen Chi ^a   Fan, Chia Kwung ^c   Su, Kua Eyre ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Cysticercosis; Granulomatous inflammation; IFN ; IL 12; OPN; Taenia solium; Th1 type responses

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; MESSENGER RNA; OSTEOPONTIN; PRAZIQUANTEL;

DEVELOPMENTAL STAGE; FLATWORM; GENE EXPRESSION; IMMUNE RESPONSE; MODELING; PARASITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIFICATION; CELL CULTURE; COCULTURE; CONTROLLED STUDY; CYSTICERCOSIS; CYSTICERCUS (CESTODE LARVA); DOWN REGULATION; FEMALE; GENE EXPRESSION; GRANULOMA; GRANULOMATOUS INFLAMMATION; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; LEUKOCYTE; METACESTODE; MOUSE; NONHUMAN; PARASITE VIABILITY; PROTEIN EXPRESSION; TAENIA SOLIUM; TH1 CELL; UPREGULATION;

ANIMALS; CYSTICERCUS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOSUPPRESSION; INTERFERON TYPE II; INTERLEUKIN-12; MICE; MICE, INBRED STRAINS; OSTEOPONTIN; TAENIA SOLIUM; TAENIASIS; TH1 CELLS;

MURINAE; TAENIA SOLIUM;

EID: 37249006454     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2007.07.010     Document Type: Article

References (50)

1. Arechavaleta F., Molinari J.L., and Tato P. A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitol. Res. 84 (1998) 117-122
2. Ashkar S., Weber G.F., Panoutsakopoulou V., Sanchirico M.E., Jansson M., Zawaideh S., Rittling S.R., Denhardt D.T., Glimcher M.J., and Cantor H. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287 (2000) 860-864
3. Atkins K., Berry J.E., Zhang W.Z., Harris J.F., Chambers A.F., Simpson R.U., and Somerman M.J. Coordinate expression of OPN and associated receptors during monocyte/macrophage differentiation of HL-60 cells. J. Cell Physiol. 175 (1998) 229-237
4. Bennett J.S., Chan C., Vilaire G., Mousa S.A., and DeGrado W.F. Agonist-activated αVβ3 on platelets and lymphocytes binds to the matrix protein osteopontin. J. Biol. Chem. 272 (1997) 8137-8140
5. Burger C.J., Rikihisa Y., and Lin Y.C. Taenia taeniaeformis: inhibition of mitogen induced proliferation and interleukin-2 production in rat splenocytes by larval in vitro product. Exp. Parasitol. 62 (1986) 216-222
6. Denhardt D.T., and Guo X. Osteopontin: a protein with diverse functions. FASEB J. 7 (1993) 1475-1482
7. Denhardt D.T., Noda M., O'Regan A.W., Pavlin D., and Berman J.S. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J. Clin. Invest. 107 (2001) 1055-1061
8. Diwan A.R., Coker-Vann M., Brown P., Subianto D.B., Yolken R., Desowitz R., Escobar A., Gibbs Jr. C.J., and Gajdusek D.C. Enzyme-linked immunosorbent assay (ELISA) for the detection of antibody to cysticerci of Taenia solium. Am. J. Trop. Med. Hyg. 31 (1982) 364-369
9. Dreweck C.M., Soboslay P.T., Schulz-Key H., Gottstein B., and Kern P. Cytokine and chemokine secretion by human peripheral blood cells in response to viable Echinococcus multilocularis metacestode vesicles. Parasite Immunol. 21 (1999) 433-438
10. Fan P.C., Chung W.C., and Wu J.C. Experimental infection of an isolate of Taenia solium from Hainan in domestic animals. J. Helminthol. 68 (1994) 265-266
11. Fan P.C., Chung W.C., Lin C.Y., and Wu C.C. Vaccination trials against Taenia solium eggs in pigs injected with frozen oncospheres of T. solium or Taenia saginata asiatica. J. Microbiol. Immunol. Infect. 36 (2003) 96-100
12. Gomez Y., Valdez R.A., Larralde C., and Romano M.C. Sex steroids and parasitism: Taenia crassiceps cisticercus metabolizes exogenous androstenedione to testosterone in vitro. J. Steroid Biochem. Mol. Biol. 74 (2000) 143-147
13. Hoffmann E., Dittrich-Breiholz O., Holtmann H., and Kracht M. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72 (2002) 847-855
14. Ito A., Chung W.C., Chen C.C., Ito M., Endo S., Okamoto M., and Fan P.C. Human Taenia eggs develop into cysticerci in scid mice. Parasitology 114 Pt 1 (1997) 85-88
15. Ito A., Ito M., Eom K.S., Chung W.C., Chen C.C., Ma L., Endo S., and Fan P.C. In vitro hatched oncospheres of Asian Taenia from Korea and Taiwan develop into cysticerci in the peritoneal cavity of female scid (severe combined immunodeficiency) mice. Int. J. Parasitol. 27 (1997) 631-633
16. Katagiri Y.U., Sleeman J., Fujii H., Herrlich P., Hotta H., Tanaka K., Chikuma S., Yagita H., Okumura K., Murakami M., Saiki I., Chambers A.F., and Uede T. CD44 variants but not CD44s cooperate with beta1-containing integrins to permit cells to bind to osteopontin independently of arginine-glycine-aspartic acid, thereby stimulating cell motility and chemotaxis. Cancer Res. 59 (1999) 219-226
17. Koguchi Y., Kawakami K., Kon S., Segawa T., Maeda M., Uede T., and Saito A. Penicillium marneffei causes osteopontin-mediated production of interleukin-12 by peripheral blood mononuclear cells. Infect. Immun. 70 (2002) 1042-1048
18. Lightowlers M.W., Mitchell G.F., Bowtell D.D., Anders R.F., and Rickard M.D. Immunization against Taenia taeniaeformis in mice: studies on the characterization of antigens from oncospheres. Int. J. Parasitol. 14 (1984) 321-333
19. Londono D.P., Alvarez J.I., Trujillo J., Jaramillo M.M., and Restrepo B.I. The inflammatory cell infiltrates in porcine cysticercosis: immunohistochemical analysis during various stages of infection. Vet. Parasitol. 109 (2002) 249-259
20. + TCRαβ T cells are critically involved in the control of experimental murine cysticercosis in C57BL/6J mice. Parasitol. Res. 87 (2001) 826-832
21. Lundahl J., Hallden G., Hallgren M., Skold C.M., and Hed J. Altered expression of CD11b/CD18 and CD62L on human monocytes after cell preparation procedures. J. Immunol. Methods 180 (1995) 93-100
22. Molinari J.L., Tato P., Reynoso O.A., and Cazares J.M. Depressive effect of a Taenia solium cysticercus factor on cultured human lymphocytes stimulated with phytohaemagglutinin. Ann. Trop. Med. Parasitol. 84 (1990) 205-208
23. Molinari J.L., Tato P., Rodriguez D., Solano S., Rubio M., and Sepulveda J. Impairment of the inflammatory reaction on implanted Taenia solium metacestodes in mice by a T. solium RNA-peptide: a scanning electron microscopy study. Parasitol. Res. 84 (1998) 173-180
24. Morales J., Velasco T., Tovar V., Fragoso G., Fleury A., Beltran C., Villalobos N., Aluja A., Rodarte L.F., Sciutto E., and Larralde C. Castration and pregnancy of rural pigs significantly increase the prevalence of naturally acquired Taenia solium cysticercosis. Vet. Parasitol. 108 (2002) 41-48
25. Nau G.J., Guilfoile P., Chupp G.L., Berman J.S., Kim S.J., Kornfeld H., and Young R.A. A chemoattractant cytokine associated with granulomas in tuberculosis and silicosis. Proc. Natl. Acad. Sci. USA 94 (1997) 6414-6419
26. O'Regan A., and Berman J.S. Osteopontin: a key cytokine in cell-mediated and granulomatous inflammation. Int. J. Exp. Pathol. 81 (2000) 373-390
27. Patarca R., Freeman G.J., Singh R.P., Wei F.Y., Durfee T., Blattner F., Regnier D.C., Kozak C.A., Mock B.A., Morse III H.C., et al. Structural and functional studies of the early T lymphocyte activation 1 (Eta-1) gene. Definition of a novel T cell-dependent response associated with genetic resistance to bacterial infection. J. Exp. Med. 170 (1989) 145-161
28. Restrepo B.I., Llaguno P., Sandoval M.A., Enciso J.A., and Teale J.M. Analysis of immune lesions in neurocysticercosis patients: central nervous system response to helminth appears Th1-like instead of Th2. J. Neuroimmunol. 89 (1998) 64-72
29. Restrepo B.I., Alvarez J.I., Castano J.A., Arias L.F., Restrepo M., Trujillo J., Colegial C.H., and Teale J.M. Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infect. Immun. 69 (2001) 4554-4560
30. Rodriguez-Sosa M., David J.R., Bojalil R., Satoskar A.R., and Terrazas L.I. Cutting edge: susceptibility to the larval stage of the helminth parasite Taenia crassiceps is mediated by Th2 response induced via STAT6 signaling. J. Immunol. 168 (2002) 3135-3139
31. Rodriguez-Sosa M., Rosas L.E., David J.R., Bojalil R., Satoskar A.R., and Terrazas L.I. Macrophage migration inhibitory factor plays a critical role in mediating protection against the helminth parasite Taenia crassiceps. Infect. Immun. 71 (2003) 1247-1254
32. Rodriguez-Sosa M., Satoskar A.R., David J.R., and Terrazas L.I. Altered T helper responses in CD40 and interleukin-12 deficient mice reveal a critical role for Th1 responses in eliminating the helminth parasite Taenia crassiceps. Int J. Parasitol. 33 (2003) 703-711
33. Rodriguez-Sosa M., Saavedra R., Tenorio E.P., Rosas L.E., Satoskar A.R., and Terrazas L.I. A STAT4-dependent Th1 response is required for resistance to the helminth parasite Taenia crassiceps. Infect. Immun. 72 (2004) 4552-4560
34. Sodek J., Batista Da Silva A.P., and Zohar R. Osteopontin and mucosal protection. J. Dent. Res. 85 (2006) 404-415
35. Spolski R.J., Corson J., Thomas P.G., and Kuhn R.E. Parasite-secreted products regulate the host response to larval Taenia crassiceps. Parasite Immunol. 22 (2000) 297-305
36. Tanaka K., Morimoto J., Kon S., Kimura C., Inobe M., Diao H., Hirschfeld G., Weiss J.M., and Uede T. Effect of osteopontin alleles on β-glucan-induced granuloma formation in the mouse liver. Am. J. Pathol. 164 (2004) 567-575
37. Tato P., Castro A.M., Rodriguez D., Soto R., Arechavaleta F., and Molinari J.L. Suppression of murine lymphocyte proliferation induced by a small RNA purified from the Taenia solium metacestode. Parasitol. Res. 81 (1995) 181-187
38. Tato P., White Jr. A.C., Willms K., Rodriguez D., Solano S., Sepulveda J., and Molinari J.L. Immunosuppression and inhibition of inflammation in mice induced by a small Taenia solium RNA-peptide to implanted T. solium metacestodes. Parasitol. Res. 82 (1996) 590-597
39. Terrazas L.I., Bojalil R., Govezensky T., and Larralde C. Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps). J. Parasitol. 84 (1998) 74-81
40. Ueno H., Murakami M., Okumura M., Kadosawa T., Uede T., and Fujinaga T. Chitosan accelerates the production of osteopontin from polymorphonuclear leukocytes. Biomaterials 22 (2001) 1667-1673
41. Ulett G.C., Ketheesan N., and Hirst R.G. Cytokine gene expression in innately susceptible BALB/c mice and relatively resistant C57BL/6 mice during infection with virulent Burkholderia pseudomallei. Infect. Immunol. 68 (2000) 2034-2042
42. Verastegui M., Gonzalez A., Gilman R.H., Gavidia C., Falcon N., Bernal T., and Garcia H.H. Experimental infection model for Taenia solium cysticercosis in swine. Cysticercosis working group in Peru. Vet. Parasitol. 94 (2000) 33-44
43. Villa O.F., and Kuhn R.E. Mice infected with the larvae of Taenia crassiceps exhibit a Th2-like immune response with concomitant anergy and downregulation of Th1-associated phenomena. Parasitology 112 (1996) 561-570
44. Wang I.C., Ma Y.X., Kuo C.H., and Fan P.C. A comparative study on egg hatching methods and oncosphere viability determination for Taenia solium eggs. Int. J. Parasitol. 27 (1997) 1311-1314
45. Wang I.C., Ma Y.X., Guo J.X., Chung W.C., Lu S.C., Ito A., and Fan P.C. Oncospheres of Taenia solium and T. saginata asiatica develop into metacestodes in normal and immunosuppressed mice. J. Helminthol. 73 (1999) 183-186
46. Wang I.C., Chung W.C., Lu S.C., and Fan P.C. Rodent model for long-term maintenance and development of the viable cysticerci of Taenia saginata asiatica. Korean J. Parasitol. 38 (2000) 237-244
47. Weber G.F., Ashkar S., Glimcher M.J., and Cantor H. Receptor-ligand interaction between CD44 and osteopontin (Eta-1). Science 271 (1996) 509-512
48. White Jr. A.C., Baig S., and Chappell C.L. Characterization of a cysteine proteinase from Taenia crassiceps cysts. Mol. Biochem. Parasitol. 85 (1997) 243-253
49. White Jr. A.C., Robinson P., and Kuhn R. Taenia solium cysticercosis: host-parasite interactions and the immune response. In: Freedman D.O. (Ed). Chemical Immunology. In Immunopathogenetic Aspects of Disease Induced by Helminth Parasites vol. 66 (1997), Karger, Basel 209-230
50. White Jr. A.C. Neurocysticercosis: updates on epidemiology, pathogenesis, diagnosis, and management. Ann. Rev. Med. 51 (2000) 187-206