Transcriptional and proteomic analysis reveal recombinant galectins of Haemonchus contortus down-regulated functions of goat PBMC and modulation of several signaling cascades in vitro

Journal of Proteomics

Volumn 98, Issue , 2014, Pages 123-137

  Wang, Wang ^a   Yuan, Cheng ^a   Wang, Shuai ^a   Song, XiaoKai ^a   Xu, LiXin ^a   Yan, RuoFeng ^a   Hasson, I A ^a   Li, XiangRui ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Galectins; Haemonchus contortus; PBMC; Signal pathway

Indexed keywords

CASPASE; GALECTIN; PROTEASOME; RECOMBINANT GALECTIN; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL MIGRATION ASSAY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE ONTOLOGY; GOAT; HAEMONCHUS CONTORTUS; IMMUNE EVASION; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEOMICS; STIMULUS RESPONSE;

GALECTINS; HAEMONCHUS CONTORTUS; PBMC; SIGNAL PATHWAY;

ANIMALS; GENE EXPRESSION REGULATION; GOAT DISEASES; GOATS; LEUKOCYTES, MONONUCLEAR; NEMATODA; NEMATODE INFECTIONS; PROTEOME; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84892877078     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.12.017     Document Type: Article

References (86)

1. Kasai K., Hirabayashi J. Galectins: a family of animal lectins that decipher glycocodes. J Biochem 1996, 119:1-8.
2. Cooper D.N. Galectinomics: finding themes in complexity. Biochim Biophys Acta 2002, 1572:209-231.
3. Vasta G.R. Roles of galectins in infection. Nat Rev Microbiol 2009, 7:424-438.
4. Mercier S., St-Pierre C., Pelletier I., Ouellet M., Tremblay M.J., Sato S. Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorption. Virology 2008, 371:121-129.
5. Mey A., Leffler H., Hmama Z., Normier G., Revillard J.P. The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J Immunol 1996, 156:1572-1577.
6. Okumura C.Y., Baum L.G., Johnson P.J. Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell Microbiol 2008, 10:2078-2090.
7. Bowater R.J., Abdelmalik S.M., Lilford R.J. The methodological quality of cluster randomised controlled trials for managing tropical parasitic disease: a review of trials published from 1998 to 2007. Trans R Soc Trop Med Hyg 2009, 103:429-436.
8. Kiel M., Josh P., Jones A., Windon R., Hunt P., Kongsuwan K. Identification of immuno-reactive proteins from a sheep gastrointestinal nematode, Trichostrongylus colubriformis, using two-dimensional electrophoresis and mass spectrometry. Int J Parasitol 2007, 37:1419-1429.
9. Turner D.G., Wildblood L.A., Inglis N.F., Jones D.G. Characterization of a galectin-like activity from the parasitic nematode, Haemonchus contortus, which modulates ovine eosinophil migration in vitro. Vet Immunol Immunopathol 2008, 122:138-145.
10. Wildblood L.A., Kerr K., Clark D.A., Cameron A., Turner D.G., Jones D.G. Production of eosinophil chemoattractant activity by ovine gastrointestinal nematodes. Vet Immunol Immunopathol 2005, 107:57-65.
11. Kim J.Y., Cho M.K., Choi S.H., Lee K.H., Ahn S.C., Kim D.H., et al. Inhibition of dextran sulfate sodium (DSS)-induced intestinal inflammation via enhanced IL-10 and TGF-beta production by galectin-9 homologues isolated from intestinal parasites. Mol Biochem Parasitol 2010, 174:53-61.
12. Hewitson J.P., Grainger J.R., Maizels R.M. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 2009, 167:1-11.
13. Li C., Li X.-R., X-F W.E.I., L-X X.U. Cloning, characterization and sequence analysis of galectin cDNA of female and male adult worms of Haemonchus contortus. J Agric Biotechnol 2005, 13:86-91.
14. Li C., Wei X., Xu L., Li X. Recombinant galectins of male and female Haemonchus contortus do not hemagglutinate erythrocytes of their natural host. Vet Parasitol 2007, 144:299-303.
15. Yan-ming S., Ruo-feng Y., Li-xin X., Muleke C.I., Xiang-rui L. Recombinant galectins of Hernonchus confortus inhibit goat cytokine mRNA transcription of peripheral blood mononuclear cells in vitro. Agric Sci China 2007, 6:1262-1268.
16. Sun Y., Yan R., Muleke C.I., Zhao G., Xu l, Li X. Recombinant galectins of Haemonchus contortus parasite induces apoptosis in the peripheral blood lymphocytes of goat. Int J Pept Res Ther 2007, 13:387-392.
17. Yanming S., Ruofeng Y., Muleke C.I., Guangwei Z., Lixin X., Xiangrui L. Vaccination of goats with recombinant galectin antigen induces partial protection against Haemonchus contortus infection. Parasite Immunol 2007, 29:319-326.
18. Rabinovich G.A., Gruppi A. Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 2005, 27:103-114.
19. Zhao G., Yan R., Muleke C.I., Sun Y., Xu L., Li X. Vaccination of goats with DNA vaccines encoding H11 and IL-2 induces partial protection against Haemonchus contortus infection. Vet J 2012, 191:94-100.
20. Han K., Xu L., Yan R., Song X., Li X. Molecular cloning, expression and characterization of enolase from adult Haemonchus contortus. Res Vet Sci 2012, 92:259-265.
21. Nicholson I.C., Mavrangelos C., Fung K., Ayhan M., Levichkin I., Johnston A., et al. Characterisation of the protein composition of peripheral blood mononuclear cell microsomes by SDS-PAGE and mass spectrometry. J Immunol Methods 2005, 305:84-93.
22. Gotz S., Garcia-Gomez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36:3420-3435.
23. Stahlberg A., Rusnakova V., Forootan A., Anderova M., Kubista M. RT-qPCR work-flow for single-cell data analysis. Methods 2013, 59:80-88.
24. Taylor D.L., Zhong L., Begg D.J., de Silva K., Whittington R.J. Toll-like receptor genes are differentially expressed at the sites of infection during the progression of Johne's disease in outbred sheep. Vet Immunol Immunopathol 2008, 124:132-151.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
26. Marinaro M., Tempesta M., Tarsitano E., Camero M., Losurdo M., Buonavoglia C., et al. Antigen-specific IFN-gamma and IL-4 production in caprine herpesvirus infected goats. Res Vet Sci 2012, 93:662-667.
27. Paclik D., Werner L., Guckelberger O., Wiedenmann B., Sturm A. Galectins distinctively regulate central monocyte and macrophage function. Cell Immunol 2011, 271:97-103.
28. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 2000, 25:25-29.
29. Rossignol M. Proteomic analysis of phosphorylated proteins. Curr Opin Plant Biol 2006, 9:538-543.
30. Deng Z., Zhang X., Tang W., Oses-Prieto J.A., Suzuki N., Gendron J.M., et al. A proteomics study of brassinosteroid response in arabidopsis. Mol Cell Proteomics 2007, 6:2058-2071.
31. Bubanovic I. 1alpha,25-dihydroxy-vitamin-D3 as new immunotherapy in treatment of recurrent spontaneous abortion. Med Hypotheses 2004, 63:250-253.
32. Willheim M., Thien R., Schrattbauer K., Bajna E., Holub M., Gruber R., et al. Regulatory effects of 1alpha,25-dihydroxyvitamin D3 on the cytokine production of human peripheral blood lymphocytes. J Clin Endocrinol Metab 1999, 84:3739-3744.
33. Pichler J., Gerstmayr M., Szepfalusi Z., Urbanek R., Peterlik M., Willheim M. 1 alpha,25(OH)2D3 inhibits not only Th1 but also Th2 differentiation in human cord blood T cells. Pediatr Res 2002, 52:12-18.
34. McInroy L., Maatta A. Down-regulation of vimentin expression inhibits carcinoma cell migration and adhesion. Biochem Biophys Res Commun 2007, 360:109-114.
35. Nieminen M., Henttinen T., Merinen M., Marttila-Ichihara F., Eriksson J.E., Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol 2006, 8:156-162.
36. Kim B.R., Jeon Y.K., Nam M.J. A mechanism of apigenin-induced apoptosis is potentially related to anti-angiogenesis and anti-migration in human hepatocellular carcinoma cells. Food Chem Toxicol 2011, 49:1626-1632.
37. Behnke J.M., Barnard C.J., Wakelin D. Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. Int J Parasitol 1992, 22:861-907.
38. Pemberton A.D., Knight P.A., Wright S.H., Miller H.R. Proteomic analysis of mouse jejunal epithelium and its response to infection with the intestinal nematode, Trichinella spiralis. Proteomics 2004, 4:1101-1108.
39. Wang Z.Q., Wang L., Cui J. Proteomic analysis of Trichinella spiralis proteins in intestinal epithelial cells after culture with their larvae by shotgun LC-MS/MS approach. J Proteomics 2012, 75:2375-2383.
40. Goldfinch G.M., Smith W.D., Imrie L., McLean K., Inglis N.F., Pemberton A.D. The proteome of gastric lymph in normal and nematode infected sheep. Proteomics 2008, 8:1909-1918.
41. Nagaraj S.H., Harsha H.C., Reverter A., Colgrave M.L., Sharma R., Andronicos N., et al. Proteomic analysis of the abomasal mucosal response following infection by the nematode, Haemonchus contortus, in genetically resistant and susceptible sheep. J Proteomics 2012, 75:2141-2152.
42. Neave M.J., Streten-Joyce C., Nouwens A.S., Glasby C.J., McGuinness K.A., Parry D.L., et al. The transcriptome and proteome are altered in marine polychaetes (Annelida) exposed to elevated metal levels. J Proteomics 2012, 75:2721-2735.
43. Kim M.H. Flavonoids inhibit VEGF/bFGF-induced angiogenesis in vitro by inhibiting the matrix-degrading proteases. J Cell Biochem 2003, 89:529-538.
44. Rousseau S., Dolado I., Beardmore V., Shpiro N., Marquez R., Nebreda A.R., et al. CXCL12 and C5a trigger cell migration via a PAK1/2-p38alpha MAPK-MAPKAP-K2-HSP27 pathway. Cell Signal 2006, 18:1897-1905.
45. McMullen M.E., Bryant P.W., Glembotski C.C., Vincent P.A., Pumiglia K.M. Activation of p38 has opposing effects on the proliferation and migration of endothelial cells. J Biol Chem 2005, 280:20995-21003.
46. Lee J.W., Kwak H.J., Lee J.J., Kim Y.N., Park M.J., Jung S.E., et al. HSP27 regulates cell adhesion and invasion via modulation of focal adhesion kinase and MMP-2 expression. Eur J Cell Biol 2008, 87:377-387.
47. Coleman J.W. Nitric oxide in immunity and inflammation. Int Immunopharmacol 2001, 1:1397-1406.
48. Kotze A.C., McClure S.J. Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. Int J Parasitol 2001, 31:1563-1571.
49. Ben-Smith A., Lammas D.A., Behnke J.M. Effect of oxygen radicals and differential expression of catalase and superoxide dismutase in adult Heligmosomoides polygyrus during primary infections in mice with differing response phenotypes. Parasite Immunol 2002, 24:119-129.
50. Colasanti M., Gradoni L., Mattu M., Persichini T., Salvati L., Venturini G., et al. Molecular bases for the anti-parasitic effect of NO (review). Int J Mol Med 2002, 9:131-134.
51. Wandurska-Nowak E. The role of nitric oxide (NO) in parasitic infections. Wiad Parazytol 2004, 50:665-678.
52. Guzik T.J., Korbut R., Adamek-Guzik T. Nitric oxide and superoxide in inflammation and immune regulation. J Physiol Pharmacol 2003, 54:469-487.
53. Sukkar S.G., Rossi E. Oxidative stress and nutritional prevention in autoimmune rheumatic diseases. Autoimmun Rev 2004, 3:199-206.
54. Del Giudice R., Monti D.M., Truppo E., Arciello A., Supuran C.T., De Simone G., et al. Human carbonic anhydrase VII protects cells from oxidative damage. Biol Chem 2013, 394:1343-1348.
55. Zimmerman U.J., Wang P., Zhang X., Bogdanovich S., Forster R. Anti-oxidative response of carbonic anhydrase III in skeletal muscle. IUBMB Life 2004, 56:343-347.
56. Nemoto-Sasaki Y., Kasai K. Deletion of lec-10, a galectin-encoding gene, increases susceptibility to oxidative stress in Caenorhabditis elegans. Biol Pharm Bull 2009, 32:1973-1977.
57. Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2001, 2:947-950.
58. Kane C.M., Cervi L., Sun J., McKee A.S., Masek K.S., Shapira S., et al. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 2004, 173:7454-7461.
59. Sun R., Zhang Y., Lv Q., Liu B., Jin M., Zhang W., et al. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by up-regulating the transactivating p63 isoform alpha (TAP63alpha). J Biol Chem 2011, 286:15918-15928.
60. Lehner M., Bailo M., Stachel D., Roesler W., Parolini O., Holter W. Caspase-8 dependent apoptosis induction in malignant myeloid cells by TLR stimulation in the presence of IFN-alpha. Leuk Res 2007, 31:1729-1735.
61. Arimilli S., Johnson J.B., Alexander-Miller M.A., Parks G.D. TLR-4 and -6 agonists reverse apoptosis and promote maturation of simian virus 5-infected human dendritic cells through NFkB-dependent pathways. Virology 2007, 365:144-156.
62. Fujita Y., Mihara T., Okazaki T., Shitanaka M., Kushino R., Ikeda C., et al. Toll-like receptors (TLR) 2 and 4 on human sperm recognize bacterial endotoxins and mediate apoptosis. Hum Reprod 2011, 26:2799-2806.
63. Bafica A., Santiago H.C., Goldszmid R., Ropert C., Gazzinelli R.T., Sher A. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J Immunol 2006, 177:3515-3519.
64. Coban C., Ishii K.J., Kawai T., Hemmi H., Sato S., Uematsu S., et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 2005, 201:19-25.
65. Jenkins S.J., Hewitson J.P., Ferret-Bernard S., Mountford A.P. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol 2005, 17:1409-1418.
66. Imtiyaz H.Z., Rosenberg S., Zhang Y., Rahman Z.S., Hou Y.J., Manser T., et al. The Fas-associated death domain protein is required in apoptosis and TLR-induced proliferative responses in B cells. J Immunol 2006, 176:6852-6861.
67. Shoshan-Barmatz V., De Pinto V., Zweckstetter M., Raviv Z., Keinan N., Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 2010, 31:227-285.
68. Abu-Hamad S., Sivan S., Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc Natl Acad Sci U S A 2006, 103:5787-5792.
69. Godbole A., Varghese J., Sarin A., Mathew M.K. VDAC is a conserved element of death pathways in plant and animal systems. Biochim Biophys Acta 2003, 1642:87-96.
70. Foger N., Rangell L., Danilenko D.M., Chan A.C. Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 2006, 313:839-842.
71. Mueller P., Massner J., Jayachandran R., Combaluzier B., Albrecht I., Gatfield J., et al. Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after T cell receptor triggering. Nat Immunol 2008, 9:424-431.
72. Kaminski S., Hermann-Kleiter N., Meisel M., Thuille N., Cronin S., Hara H., et al. Coronin 1A is an essential regulator of the TGFbeta receptor/SMAD3 signaling pathway in Th17 CD4(+) T cells. J Autoimmun 2011, 37:198-208.
73. Amsen D., Blander J.M., Lee G.R., Tanigaki K., Honjo T., Flavell R.A. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 2004, 117:515-526.
74. Szabo S.J., Kim S.T., Costa G.L., Zhang X., Fathman C.G., Glimcher L.H. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000, 100:655-669.
75. Lee H.J., Takemoto N., Kurata H., Kamogawa Y., Miyatake S., O'Garra A., et al. GATA-3 induces T helper cell type 2 (Th2) cytokine expression and chromatin remodeling in committed Th1 cells. J Exp Med 2000, 192:105-115.
76. Flynn R.J., Mulcahy G. Possible role for Toll-like receptors in interaction of Fasciola hepatica excretory/secretory products with bovine macrophages. Infect Immun 2008, 76:678-684.
77. Donnelly S., O'Neill S.M., Sekiya M., Mulcahy G., Dalton J.P. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect Immun 2005, 73:166-173.
78. Gigante M., Ranieri E. TGF-beta promotes immune suppression by inhibiting Treg cell apoptosis. Immunotherapy 2010, 2:608.
79. Coux O., Tanaka K., Goldberg A.L. Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 1996, 65:801-847.
80. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001, 83:301-310.
81. Reinstein E., Ciechanover A. Narrative review: protein degradation and human diseases: the ubiquitin connection. Ann Intern Med 2006, 145:676-684.
82. Powell S.R., Wang P., Divald A., Teichberg S., Haridas V., McCloskey T.W., et al. Aggregates of oxidized proteins (lipofuscin) induce apoptosis through proteasome inhibition and dysregulation of proapoptotic proteins. Free Radic Biol Med 2005, 38:1093-1101.
83. Zhang Y., Jia L., Lee S.J., Wang M.M. Conserved signal peptide of Notch3 inhibits interaction with proteasome. Biochem Biophys Res Commun 2007, 355:245-251.
84. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005, 5:749-759.
85. Gilmore T.D. The Re1/NF-kappa B/I kappa B signal transduction pathway and cancer. Cancer Treat Res 2003, 115:241-265.
86. Puneet P., McGrath M.A., Tay H.K., Al-Riyami L., Rzepecka J., Moochhala S.M., et al. The helminth product ES-62 protects against septic shock via Toll-like receptor 4-dependent autophagosomal degradation of the adaptor MyD88. Nat Immunol 2011, 12:344-351.