Hepatic gene expression profile in mice perorally infected with Echinococcus multilocularis eggs

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Gottstein, Bruno ^a   Wittwer, Matthias ^a   Schild, Marc ^a   Merli, Michael ^b   Leib, Stephen L ^a   Müller, Norbert ^a   Müller, Joachim ^a   Jaggi, Rolf ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD74 ANTIGEN; CXCL9 CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DECTIN 1; FIBRINOGEN; FIBRINOGEN LIKE PROTEIN 2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; HEXOKINASE III; INTERLEUKIN 2 RECEPTOR GAMMA; LECTIN; LECTIN GALACTOSE BINDING SOLUBLE 3; LIPOPROTEIN LIPASE; LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN 86; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE 1; MEMBRANE COFACTOR PROTEIN; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL RESIDENT PROTEIN ES1; PLECKSTRIN; RANTES; RGS2 PROTEIN; RIBOSOME PROTEIN; RIBOSOME PROTEIN 23; RIBOSOME PROTEIN 37; STAT1 PROTEIN; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; BIOLOGICAL MARKER; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE COURSE; DNA MICROARRAY; ECHINOCOCCOSIS; ECHINOCOCCUS MULTILOCULARIS; EOSINOPHIL; FEMALE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENETIC ASSOCIATION; IMMUNE RESPONSE; IMMUNOSTIMULATION; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTE; MICROFLUIDIC ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; REAL TIME POLYMERASE CHAIN REACTION; VALIDATION PROCESS; ANIMAL; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INSTRUMENTATION; LIVER; LIVER DISEASE; METABOLISM; METHODOLOGY; OOCYTE; PARASITOLOGY;

ECHINOCOCCUS MULTILOCULARIS; MUS;

ANIMALS; BIOLOGICAL MARKERS; ECHINOCOCCOSIS; ECHINOCOCCUS MULTILOCULARIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS; LIVER; LIVER DISEASES; MICE; OVUM; RNA, MESSENGER;

EID: 77956359524     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009779     Document Type: Article

References (74)

1. Gottstein B, Piarroux R (2008) Current trends in tissue-affecting helminths. Parasite 15: 291-298.
2. nd edition, eds. GC Cook and AI Zumla, Saunders Elsevier Ltd. chapter 86: 1549-1568.
3. Siles-Lucas M, Merli M, Mackenstedt U, Gottstein B (2003) The Echinococcus multilocularis 14-3-3 protein protects mice against primary but not secondary alveolar echinococcosis. Vaccine 21: 431-439.
4. Parasite Immunol 20: 623-629.
5. Gauci C, Merli M, Muller V, Chow C, Yagi K, et al. (2002) Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infect Immun 70: 3969-3972.
6. Bauder B, Auer H, Schilcher F, Gabler C, Romig T, et al. (1999) Experimental investigations on the B and T cell immune response in primary alveolar echinococcosis. Parasite Immunol 21: 409-421.
7. Zhao Y, Ferguson DJ, Wilson DC, Howard JC, Sibley LD, et al. (2009) Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages. J Immunol 182: 3775-3781.
8. Weinländer K, Naschberger E, Lehmann MH, Tripal P, Paster W, et al. (2008) Guanylate binding protein-1 inhibits spreading and migration of endothelial cells through induction of integrin alpha4 expression. FASEB J 22: 4168-4178.
9. Degrandi D, Konermann C, Beuter-Gunia C, Kresse A, Würthner J, et al. (2007) Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J Immunol 179: 7729-7740.
10. Schnoor M, Betanzos A, Weber DA, Parkos CA (2009) Guanylate-binding protein-1 is expressed at tight junctions of intestinal epithelial cells in response to interferon-gamma and regulates barrier function through effects on apoptosis. Mucosal Immunol 2: 33-42.
11. Brännström A, Sankala M, Tryggvason K, Pikkarainen T (2002) Arginine residues in domain V have a central role for bacteria-binding activity of macrophage scavenger receptor MARCO. Biochem Biophys Res Commun 290: 1462-1469.
12. Bandyopadhyay SK, de la Motte CA, Kessler SP, Hascall VC, Hill DR, et al. (2008) Hyaluronan-mediated leukocyte adhesion and dextran sulfate sodiuminduced colitis are attenuated in the absence of signal transducer and activator of transcription 1. Am J Pathol 173: 1361-1368.
13. Neufert C, Becker C, Wirtz S, Fantini MC, Weigmann B, et al. (2007) IL-27 controls the development of inducible regulatory T cells and Th17 cells via differential effects on STAT1. Eur J Immunol 37: 1809-1816.
14. Ramsauer K, Farlik M, Zupkovitz G, Seiser C, Kröger A, et al. (2007) Distinct modes of action applied by transcription factors STAT1 and IRF1 to initiate transcription of the IFN-gamma-inducible gbp2 gene. Proc Natl Acad Sci U S A 104: 2849-2854.
15. Jeong WI, Park O, Radaeva S, Gao B (2006) STAT1 inhibits liver fibrosis in mice by inhibiting stellate cell proliferation and stimulating NK cell cytotoxicity. Hepatology 44: 1441-1451.
16. Shuai K (2000) Modulation of STAT signaling by STAT-interacting proteins. Oncogene 19: 2638-2644.
17. Ramsey C, Rubinstein MP, Kim DM, Cho JH, Sprent J, et al. (2008) The lymphopenic environment of CD132 (common gamma-chain)-deficient hosts elicits rapid homeostatic proliferation of naive T cells via IL-15. J Immunol 180: 5320-5326.
18. Xiao H, Yin T, Wang XY, Uchida T, Chung J, et al. (2002) Specificity of interleukin-2 receptor gamma chain superfamily cytokines is mediated by insulin receptor substrate-dependent pathway. J Biol Chem 277: 8091-8098.
19. Hawkins PT, Stephens LR (2007) PI3Kgamma is a key regulator of inflammatory responses and cardiovascular homeostasis. Science 318: 64-66.
20. MacKinnon AC, Farnworth SL, Hodkinson PS, Henderson NC, Atkinson KM, et al. (2008) Regulation of alternative macrophage activation by galectin-3. J Immunol 180: 2650-2658.
21. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197: 1107-1117.
22. Liu N, Wang Y, Ashton-Rickardt PG (2004) Serine protease inhibitor 2A inhibits caspase-independent cell death. FEBS Lett 569: 49-53.
23. Faure-André G, Vargas P, Yuseff MI, Heuzé M, Diaz J, et al. (2008) Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. Science 322: 1705-1710.
24. Manicone AM, Burkhart KM, Lu B, Clark JG (2008) CXCR3 ligands contribute to Th1-induced inflammation but not to homing of Th1 cells into the lung. Exp Lung Res 34: 391-407.
25. Zhai Y, Shen XD, Gao F, Zhao A, Freitas MC, et al. (2008) CXCL10 regulates liver innate immune response against ischemia and reperfusion injury. Hepatology 47: 207-214.
26. Nakamichi K, Inoue S, Takasaki T, Morimoto K, Kurane I (2004) Rabies virus stimulates nitric oxide production and CXC chemokine ligand 10 expression in macrophages through activation of extracellular signal-regulated kinases 1 and 2. J Virol 78: 9376-9388.
27. Koniaris LG, Zimmers-Koniaris T, Hsiao EC, Chavin K, Sitzmann JV, et al. (2001) Cytokine-responsive gene-2/IFN-inducible protein-10 expression in multiple models of liver and bile duct injury suggests a role in tissue regeneration. J Immunol 167: 399-406.
28. Santiago HC, Oliveira CF, Santiago L, Ferraz FO, de Souza DG, et al. (2004) Involvement of the chemokine RANTES (CCL5) in resistance to experimental infection with Leishmania major. Infect Immun 72: 4918-4923.
29. Xu H, Williams MS, Spain LM (2006) Patterns of expression, membrane localization, and effects of ectopic expression suggest a function for MS4a4B, a CD20 homolog in Th1 T cells. Blood 107: 2400-2408.
30. Fujiwara K, Daido S, Yamamoto A, Kobayashi R, Yokoyama T, et al. (2008) Pivotal role of the cyclin-dependent kinase inhibitor p21WAF1/CIP1 in apoptosis and autophagy. J Biol Chem 283: 388-397.
31. Hui L, Zatloukal K, Scheuch H, Stepniak E, Wagner EF (2008) Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1- dependent p21 downregulation. J Clin Invest 118: 3943-3953.
32. Asefa B, Dermott JM, Kaldis P, Stefanisko K, Garfinkel DJ, et al. (2006) p205, a potential tumor suppressor, inhibits cell proliferation via multiple pathways of cell cycle regulation. FEBS Lett 580: 1205-1214.
33. Nagai Y, Shimazu R, Ogata H, Akashi S, Sudo K, et al. (2002) Requirement for MD-1 in cell surface expression of RP105/CD180 and B-cell responsiveness to lipopolysaccharide. Blood 99: 1699-1705.
34. Shalev I, Wong KM, Foerster K, Zhu Y, Chan C, et al. (2009) The novel CD4+CD25+ regulatory T cell effector molecule fibrinogen-like protein 2 contributes to the outcome of murine fulminant viral hepatitis. Hepatology 49: 387-397.
35. Liu H, Shalev I, Manuel J, He W, Leung E, et al. (2008) The FGL2- FcgammaRIIB pathway: a novel mechanism leading to immunosuppression. Eur J Immunol 38: 3114-3126.
36. Stanley AC, Dalton JE, Rossotti SH, MacDonald KP, Zhou Y, et al. (2008) VCAM-1 and VLA-4 modulate dendritic cell IL-12p40 production in experimental visceral leishmaniasis. PLoS Pathog 19 4(9): e1000158.
37. Bansal G, Druey KM, Xie Z (2007) R4 RGS proteins: regulation of G-protein signaling and beyond. Pharmacol Ther 116: 473-495.
38. Yang D, Chen Q, Su SB, Zhang P, Kurosaka K, et al. (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.
39. Nakajima M, Hirakata M, Nittoh T, Ishihara K, Ohuchi K (2001) Expression and purification of recombinant rat eosinophil-associated ribonucleases, homologues of human eosinophil cationic protein and eosinophil-derived neurotoxin, and their characterization. Int Arch Allergy Immunol 125: 241-249.
40. Yang D, Rosenberg HF, Chen Q, Dyer KD, Kurosaka K, et al. (2003) Eosinophil-derived neurotoxin (EDN), an antimicrobial protein with chemotactic activities for dendritic cells. Blood 102: 3396-3403.
41. Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80: 753-769.
42. Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057.
43. Fujii C, Nakamoto Y, Lu P, Tsuneyama K, Popivanova BK, et al. (2005) Aberrant expression of serine/threonine kinase Pim-3 in hepatocellular carcinoma development and its role in the proliferation of human hepatoma cell lines. Int J Cancer 114: 209-218.
44. Macdonald A, Campbell DG, Toth R, McLauchlan H, Hastie CJ, et al. (2006) Pim kinases phosphorylate multiple sites on Bad and promote 14-3-3 binding and dissociation from Bcl-XL. BMC Cell Biol 10 7: 1.
45. Agnihotri G, Liu HW (2003) Enoyl-CoA hydratase. reaction, mechanism, and inhibition. Bioorg Med Chem 11: 9-20.
46. Bresson-Hadni S, Liance M, Meyer JP, Houin R, Bresson JL, et al. (1990) Cellular immunity in experimental Echinococcus multilocularis infection. II. Sequential and comparative phenotypic study of the periparasitic mononuclear cells in resistant and sensitive mice. Clin Exp Immunol 82: 378-383.
47. Emery I, Liance M, Deriaud E, Vuitton DA, Houin R, et al. (1996) Characterization of T-cell immune responses of Echinococcus multilocularisinfected C57BL/6J mice. Parasite Immunol 18: 463-472.
48. Playford MC, Kamiya M (1992) Immune respoflse to Echinococcus multilocularis infection in the mouse model. Jpn J Vet Res 40: 113-130.
49. Playford MC, Ooi HK, Oku Y, Kamiya M (1992) Secondary Echinococcus multilocularis infection in severe combined immunodeficient (scid) mice: biphasic growth of the larval cyst mass. Int J Parasitol 22: 975-982.
50. Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, et al. (1997) Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 130: 320-323.
51. Zingg W, Renner-Schneiter EC, Pauli-Magnus C, Renner EL, van Overbeck J, et al. (2002) Alveolar echinococcosis of the liver in an adult with human immunodeficiency virus type-1 infection. Infection 32: 299-302.
52. Liance M, Aicard-Blum S, Emery I, Houin A, Vuitton DA (1998) Echinococcus multilocularis infection in mice: in vivo treatment with a low dose of IFN-gamma decreases metacestode growth and liver fibrogenesis. Parasite 5: 231-237.
53. Jenne L, Kilwinski J, Aadloff P, Flick W, Kern P (1998) Clinical efficacy of and immunologic alterations caused by interferon gamma therapy for alveolar echinococcosis. Clin Infect Dis 26: 492-494.
54. Amiot F, Vuong P, Defontaines M, Pater C, Dautry F, et al. (1999) Secondary alveolar echinococcosis in Iymphotoxinalpha and tumour necrosis factor-alpha deficient mice: exacerbation of Echinococcus multilocularis larval growth is associated with cellular changes in the periparasitic granuloma. Parasite Immunol 21: 475-483.
55. Godot V, Harraga S, Podoprigora G, Liance M, Bardonnet K, et al. (2003) IFN alpha-2a protects mice against a helminth infection of the liver and modulates immune responses. Gastroenterol 124: 1441-1450.
56. Emery I, Leclerc C, Sengphommachanh K, Vuitton DA, Liance M (1998) In vivo treatment with recombinant IL-12 protects C57BL/6J mice against secondary alveolar echinococcosis. Parasite Immunol 20: 81-91.
57. Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85: 119-132.
58. Dai WJ, Waldvogel A, Jungi T, Stettler M, Gottstein B (2003) Inducible nitric oxide synthase-deficiency in mice increases resistance to chronic infection with Echinococcus multilocularis. Immunol 10: 238-244.
59. Mejri N, Gottstein B (2006) Intraperitoneal Echinococcus multilocularis infection in C57BL/6 mice inhibits the up-regulation of B7-1 and B7-2 co-stimulator expression on peritoneal macrophages and causes failure to enhance peritoneal T cell activation. Parasite Immunol 28: 373-385.
60. Mejri N, Gottstein B (2009) Echinococcus multilocularis metacestode metabolites contain a cysteine protease that digests eotaxin, a CC pro-inflammatory chemokine. Parasitol Res, Jul 2 [Epub ahead of print].
61. Pennock JL, Grencis RK (2006) The mast cell and gut nematodes: damage and defence. Chem Immunol Allergy 90: 128-140.
62. Baron RW, Tanner CE (1976) The effect of immunosuppression on secondary Echinococcus multilocularis infections in mice. Int J Parasitol 6: 37-42.
63. Devouge M, Ali-Khan Z (1983) Intraperitoneal murine alveolar hydatidosis: relationship between the size of the larval cyst mass, immigrant inflammatory cells, splenomegaly and thymus involution. Tropenmed Parasito! 34: 15-20.
64. Kizaki T, Ishige M, Bingyan W, Day NK, Good RA, et al. (1993) Generation of CD8+ suppressor T cells by proto scoleces of Echinococcus multilocularis in vitro. Immunol 79: 412-417.
65. Stanley AC, Dalton JE, Rossotti SH, MacDonald KP, Zhou Y, et al. (2008) VCAM-1 and VLA-4 modulate dendritic cell IL-12p40 production in experimental visceral leishmaniasis. PLoS Pathog 19: e1000158.
66. Vuitton DA, Zhang SL, Yang Y, Godot V, Beurton I, et al. (2006) Survival strategy of Echinococcus multilocularis in the human host. Parasitol 55: S51-S55.
67. Bernthaler P, Epping K, Schmitz G, Deplazes P, Brehm K (2009) Molecular characterization of EmABP, an apolipoprotein A-I binding protein secreted by the Echinococcus multilocularis metacestode. Infect Immun 77: 5564-5571.
68. McManus DP (2009) Reflections on the biochemistry of Echinococcus: past, present and future. Parasitology 136: 1643-1652.
69. Vuitton DA, Guerret-Stocker S, Carbillet JP, Mantion G, Miguet JP, et al. (1986) Collagen immunotyping of the hepatic fibrosis in human alveolar echinococcosis. Z Parasitenkd 72: 97-104.
70. Pater C, Müller V, Harraga S, Liance M, Godot V, et al. (1998) Intestinal and systemic humoral immunological events in the susceptible Balb/C mouse strain after oral administration of Echinococcus multilocularis eggs.
71. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
72. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
73. Kooperberg C, Aragaki A, Strand AD, Olson JM (2005) Significance testing for small microarray experiments. Stat Med 24: 2281-2298.
74. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.