Eimeria bovis-induced modulation of the host cell proteome at the meront I stage

Molecular and Biochemical Parasitology

Volumn 175, Issue 1, 2011, Pages 1-9

  Lutz, Kathleen ^a   Schmitt, Sigrid ^a   Linder, Monica ^a   Hermosilla, Carlos ^b   Zahner, Horst ^a   Taubert, Anja ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Apicomplexa; Eimeria bovis; First merogony; Host cell; Proteome

Indexed keywords

ALPHA ACTININ 1; CASPASE 8; CELL PROTEIN; GELSONIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEOME; TRANSGELIN; TROPOMODULIN 3; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL METABOLISM; CELL STRUCTURE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; COW; DEPOLYMERIZATION; DOWN REGULATION; EIMERIA BOVIS; GENETIC TRANSCRIPTION; HOST CELL; HOST PARASITE INTERACTION; MEROZOITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; SCHIZONT; UPREGULATION;

ANIMALS; CATTLE; CELLS, CULTURED; DOWN-REGULATION; EIMERIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EPITHELIAL CELLS; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; UP-REGULATION;

APICOMPLEXA; EIMERIA; EIMERIA BOVIS;

EID: 78049431358     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2010.08.003     Document Type: Article

References (65)

1. Daugschies A., Najdrowski M. Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 2005, 52:417-427.
2. Nyberg P.A., Hammond D.M. Description of the sporulated oozysts and sporozoites of four species of bovine coccidia. J Parasitol 1965, 51:669-673.
3. Hammond D.M., Ernst J.V., Miner M.L. The development of first generation schizonts of Eimeria bovis. J Protozool 1966, 13:559-564.
4. Hammond D.M., Fayer R. Cultivation of Eimeria bovis in three established cell lines and in bovine tracheal cell line cultures. J Parasitol 1968, 54:559-568.
5. Coppens I., Sinai A.P., Joiner K.A. Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 2000, 149:167-180.
6. Sinai A.P., Joiner K.A. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu Rev Microbiol 1997, 51:415-462.
7. Frias M.A., Rebsamen M.C., Gerber-Wicht C., et al. Prostaglandin E2 activates Stat3 in neonatal rat ventricular cardiomyocytes: a role in cardiac hypertrophy. Cardiovasc Res 2007, 73:57-65.
8. Fisch S., Gray S., Heymans S., et al. Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 2007, 104:7074-7079.
9. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 2000, 102:1-4.
10. Laliberte J., Carruthers V.B. Host cell manipulation by the human pathogen Toxoplasma gondii. Cell Mol Life Sci 2008.
11. Martin A.M., Liu T., Lynn B.C., et al. The Toxoplasma gondii parasitophorous vacuole membrane: transactions across the border. J Eukaryot Microbiol 2007, 54:25-28.
12. Sinai A.P., Joiner K.A. The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 2001, 154:95-108.
13. Vutova P., Wirth M., Hippe D., et al. Toxoplasma gondii inhibits Fas/CD95-triggered cell death by inducing aberrant processing and degradation of caspase 8. Cell Microbiol 2007, 9:1556-1570.
14. Keller P., Schaumburg F., Fischer S.F., et al. Direct inhibition of cytochrome c-induced caspase activation in vitro by Toxoplasma gondii reveals novel mechanisms of interference with host cell apoptosis. FEMS Microbiol Lett 2006, 258:312-319.
15. Molestina R.E., Payne T.M., Coppens I., et al. Activation of NF-kappaB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. J Cell Sci 2003, 116:4359-4371.
16. Hermosilla C., Schröpfer E., Stowasser M., et al. Cytoskeletal changes in Eimeria bovis-infected host endothelial cells during first merogony. Vet Res Commun 2008.
17. Lang M., Kann M., Zahner H., et al. Inhibition of host cell apoptosis by Eimeria bovis sporozoites. Vet Parasitol 2009, 160:25-33.
18. del Cacho E., Gallego M., Lopez-Bernad F., et al. Expression of anti-apoptotic factors in cells parasitized by second-generation schizonts of Eimeria tenella and Eimeria necatrix. Vet Parasitol 2004, 125:287-300.
19. Alcala-Canto Y., Ibarra-Velarde F. Cytokine gene expression and NF-kappaB activation following infection of intestinal epithelial cells with Eimeria bovis or Eimeria alabamensis in vitro. Parasite Immunol 2008, 30:175-179.
20. Hermosilla C., Zahner H., Taubert A. Eimeria bovis modulates adhesion molecule gene transcription in and PMN adhesion to infected bovine endothelial cells. Int J Parasitol 2006, 36:423-431.
21. Taubert A., Zahner H., Hermosilla C. Eimeria bovis infection enhances adhesion of peripheral blood mononuclear cells to and their transmigration through an infected bovine endothelial cell monolayer in vitro. Parasitol Res 2007, 101:591-598.
22. Taubert A., Hermosilla C., Behrendt J., et al. Responses of bovine endothelial cells in vitro to coccidia (Eimeria bovis, Toxoplasma gondii, Neospora caninum) infections possibly involved in innate immunity. Berl Münch Tierarztl Wochenschr 2006, 119:274-281.
23. Taubert A., Zahner H., Hermosilla C. Dynamics of transcription of immunomodulatory genes in endothelial cells infected with different coccidian parasites. Vet Parasitol 2006, 142:214-222.
24. Fiege N., Klatte D., Kollmann D., et al. Eimeria bovis in cattle: colostral transfer of antibodies and immune response to experimental infections. Parasitol Res 1992, 78:32-38.
25. Jackson A.R. The isolation of viable coccidial sporozoites. Parasitology 1964, 54:87-93.
26. Hermosilla C., Barbisch B., Heise A., et al. Development of Eimeria bovis in vitro: suitability of several bovine, human and porcine endothelial cell lines, bovine fetal gastrointestinal, Madin-Darby bovine kidney (MDBK) and African green monkey kidney (VERO) cells. Parasitol Res 2002, 88:301-307.
27. Hermosilla C., Stamm I., Taubert A., et al. Fluorescent Eimeria bovis sporozoites and meront stages in vitro: a helpful tool to study parasite-host cell interactions. Parasitol Res 2008, 102:777-786.
28. Forst C.V. Host-pathogen systems biology. Drug Discov Today 2006, 11:220-227.
29. Krug E.C., Marr J.J., Berens R.L. Purine metabolism in Toxoplasma gondii. J Biol Chem 1989, 264:10601-10607.
30. Sibley L.D. No more free lunch. Nature 2002, 415:843-844.
31. Nelson M.M., Jones A.R., Carmen J.C., et al. Modulation of the host cell proteome by the intracellular apicomplexan parasite Toxoplasma gondii. Infect Immun 2008, 76:828-844.
32. Gruenbaum Y., Wilson K.L., Harel A., et al. Review: nuclear lamins-structural proteins with fundamental functions. J Struct Biol 2000, 129:313-323.
33. Ottaviano Y., Gerace L. Phosphorylation of the nuclear lamins during interphase and mitosis. J Biol Chem 1985, 260:624-632.
34. Titus M.A. Cell biology: myosins meet microtubules. Nature 2004, 431:252-253.
35. Woolner S., O'Brien L.L., Wiese C., et al. Myosin-10 and actin filaments are essential for mitotic spindle function. J Cell Biol 2008, 182:77-88.
36. Moore M.S., Blobel G. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 1993, 365:661-663.
37. Pemberton L.F., Paschal B.M. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005, 6:187-198.
38. Dreyfuss G., Matunis M.J., Pinol-Roma S., et al. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 1993, 62:289-321.
39. Pinol-Roma S., Dreyfuss G. hnRNP proteins: localization and transport between the nucleus and the cytoplasm. Trends Cell Biol 1993, 3:151-155.
40. Lu X., Legerski R.J. The Prp19/Pso4 core complex undergoes ubiquitylation and structural alterations in response to DNA damage. Biochem Biophys Res Commun 2007, 354:968-974.
41. +/calmodulin-binding protein cleaved by caspases. Biochem Biophys Res Commun 2007, 361:281-286.
42. Chen X.M., Levine S.A., Splinter P.L., et al. Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 2001, 120:1774-1783.
43. Heussler V.T., Kuenzi P., Rottenberg S. Inhibition of apoptosis by intracellular protozoan parasites. Int J Parasitol 2001, 31:1166-1176.
44. Heussler V.T., Machado J., Fernandez P.C., et al. The intracellular parasite Theileria parva protects infected T cells from apoptosis. Proc Natl Acad Sci USA 1999, 96:7312-7317.
45. Kuenzi P., Schneider P., Dobbelaere D.A. Theileria parva-transformed T cells show enhanced resistance to Fas/Fas ligand-induced apoptosis. J Immunol 2003, 171:1224-1231.
46. Dobbelaere D.A., Kuenzi P. The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Curr Opin Immunol 2004, 16:524-530.
47. Caamano J., Tato C., Cai G., et al. Identification of a role for NF-kappa B2 in the regulation of apoptosis and in maintenance of T cell-mediated immunity to Toxoplasma gondii. J Immunol 2000, 165:5720-5728.
48. Lüder C.G., Gross U. Apoptosis and its modulation during infection with Toxoplasma gondii: molecular mechanisms and role in pathogenesis. Curr Top Microbiol Immunol 2005, 289:219-237.
49. Carmen J.C., Hardi L., Sinai A.P. Toxoplasma gondii inhibits ultraviolet light-induced apoptosis through multiple interactions with the mitochondrion-dependent programmed cell death pathway. Cell Microbiol 2006, 8:301-315.
50. Nishikawa Y., Mishima M., Nagasawa H., et al. Interferon-gamma-induced apoptosis in host cells infected with Neospora caninum. Parasitology 2001, 123:25-31.
51. Nishikawa Y., Makala L., Otsuka H., et al. Mechanisms of apoptosis in murine fibroblasts by two intracellular protozoan parasites, Toxoplasma gondii and Neospora caninum. Parasite Immunol 2002, 24:347-354.
52. Herman R.K., Molestina R.E., Sinai A.P., et al. The apicomplexan pathogen Neospora caninum inhibits host cell apoptosis in the absence of discernible NF-kappa B activation. Infect Immun 2007, 75:4255-4262.
53. Graumann K., Hippe D., Gross U., et al. Mammalian apoptotic signalling pathways: multiple targets of protozoan parasites to activate or deactivate host cell death. Microbes Infect 2009, 11:1079-1087.
54. Duckett C.S., Nava V.E., Gedrich R.W., et al. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 1996, 15:2685-2694.
55. Liston P., Roy N., Tamai K., et al. Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 1996, 379:349-353.
56. Deveraux Q.L., Reed J.C. IAP family proteins-suppressors of apoptosis. Genes Dev 1999, 13:239-252.
57. Irmler M., Thome M., Hahne M., et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997, 388:190-195.
58. Bratton S.B., Walker G., Srinivasula S.M., et al. Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J 2001, 20:998-1009.
59. Micheau O., Thome M., Schneider P., et al. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J Biol Chem 2002, 277:45162-45171.
60. Scarabelli T.M., Knight R., Stephanou A., et al. Clinical implications of apoptosis in ischemic myocardium. Curr Probl Cardiol 2006, 31:181-264.
61. Golks A., Brenner D., Krammer P.H., et al. The c-FLIP-NH2 terminus (p22-FLIP) induces NF-kappaB activation. J Exp Med 2006, 203:1295-1305.
62. Beere H.M., Wolf B.B., Cain K., et al. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2000, 2:469-475.
63. Beere H.M. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 2005, 115:2633-2639.
64. Sampson M.J., Lovell R.S., Craigen W.J. Isolation, characterization, and mapping of two mouse mitochondrial voltage-dependent anion channel isoforms. Genomics 1996, 33:283-288.
65. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999, 341(Pt 2):233-249.