Impairment of dendritic cell function and induction of CD4+CD25+Foxp3+ T cells by excretory-secretory products: A potential mechanism of immune evasion adopted by Echinococcus granulosus

BMC Immunology

Volumn 16, Issue 1, 2015, Pages

  Wang, Ying ^a,b   Zhou, Hejun ^a,b   Shen, Yujuan ^a,b   Wang, Yanjuan ^a,b   Wu, Weiping ^a,b   Liu, Haipeng ^a,b   Yuan, Zhongying ^a,b   Xu, Yuxin ^a,b   Hu, Yuan ^a,b   Cao, Jianping ^a,b  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b WHO Collaborating Center for Malaria Schistosomiasis and Filariasis   (China)

Author keywords

Cytokine; Dendritic cell; Dendritic cell maturation; Echinococcus granulosus; Excretory secretory products; Mechanism

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; EXCRETORY SECRETORY PRODUCT; GAMMA INTERFERON; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NATURAL PRODUCTS AND THEIR SYNTHETIC DERIVATIVES; PARASITE ANTIGEN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; LIGAND; OVALBUMIN; TOLL LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL MATURATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ECHINOCOCCUS GRANULOSUS; IMMUNE EVASION; IMMUNOMODULATION; IN VITRO STUDY; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW CELL; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHENOTYPE; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; ANTIGENS, HELMINTH; BONE MARROW CELLS; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; ECHINOCOCCUS GRANULOSUS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE EVASION; LIGANDS; MICE, INBRED BALB C; MICE, TRANSGENIC; OVALBUMIN; PHENOTYPE; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS;

EID: 84938929458     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/s12865-015-0110-3     Document Type: Article

References (43)

1. Moro P, Schantz PM. Echinococcosis: a review. Int J Infect Dis. 2009;3:125-33.
2. Siracusano A, Rigano R, Ortona E, Profumo E, Margutti P, Buttari B, et al. Immunomodulatory mechanisms during Echinococcus granulosus infection. Exp Parasitol. 2008;119:483-9.
3. Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol. 2009;167:1-11.
4. Johnston MJ, MacDonald JA, McKay DM. Parasitic helminths: a pharmacopeia of anti-inflammatory molecules. Parasitology. 2009;136:125-47.
5. Van Hellemond JJ, Retra K, Brouwers JF, van Balkom BW, Yazdanbakhsh M, Shoemaker CB, et al. Functions of the tegument of schistosomes: clues from the proteome and lipidome. Int J Parasitol. 2006;36:691-9.
6. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245-52.
7. Steinman RM. Dendritic cells. In: Paul WE, editor. Fundamental Immunolog. 4th ed. Philadelphia, PA: Lippincott-Raven Publishers; 1991. p. 547-73.
8. Kanan JHC, Chain BM. Modulation of dendritic cell differentiation and cytokine secretion by the hydatid cyst fluid of Echinococcus granulosus. Immunology. 2006;118:271-8.
9. Rigano R, Buttari B, Profumo E, Ortona E, Delunardo F, Margutti P, et al. Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infect Immun. 2007;75:1667-78.
10. Casaravilla C, Pittini A, Ruickerl D, Seoane PI, Jenkins SJ, MacDonald AS, et al. Unconventional maturation of dendritic cells induced by particles from the laminated layer of larval Echinococcus granulosus. Infect Immun. 2014;82:3164-76.
11. Nono JK, Pletinckx K, Lutz MB, Brehm K. Excretory/secretory-products of Echinococcus multilocularis larvae induce apoptosis and tolerogenic properties in dendritic cells in vitro. PLoS Negl Trop Dis. 2012;6:e1516.
12. Pan W, Zhou HJ, Shen YJ, Wang Y, Xu YX, Hu Y, et al. Surveillance on the status of immune cells after Echinococcus granulosus protoscoleces infection in Balb/c mice. PLoS ONE. 2013;8:e59746.
13. Inaba KM, Inaba N, Romani H, Aya H, Dequchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/ macrophage colony stimulating factor. J Exp Med. 1992;176:1693-702.
14. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods. 1999;223:77-92.
15. Chemale G, van Rossum AJ, Jefferies JR, Barrett J, Brophy PM, Ferreira HB, et al. Proteomic analysis of the larval stage of the parasite Echinococcus granulosus: Causative agent of cystic hydatid disease. Proteomics. 2003;3:1633-6.
16. Monteiro KM, de Carvalho MO, Zaha A, Ferreira HB. Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics. 2010;10:1985-99.
17. Aziz A, Zhang W, Li J, Loukas A, McManus DP, Mulvenna J. Proteomic characterization of Echinococcus granulosus hydatid cyst fluid from sheep, cattle and humans. J Proteomics. 2011;74:1560-72.
18. Virginio VG, Monteiro KM, Drumond F, de Carvalho MO, Vargas DM, Zaha A, et al. Excretory/secretory products from in vitro-cultured Echinococcus granulosus protoscoleces. Mol Biochem Parasitol. 2012;183:15-22.
19. Siracusano A, Margutti P, Delunardo F, Profumo E, Rigano R, Buttari B, et al. Molecular cross-talk in host-parasite relationships: the intriguing immunomodulatory role of Echinococcus antigen B in cystic echinococcosis. Inter J Parasitol. 2008;38:1371-6.
20. Shepherd CS, Kitken A, McManus DP. A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Mol Biochem Parasitol. 1991;44:81-90.
21. Rigano R, Profumo E, Bruschi F, Carulli G, Azzara A, Ioppolo S, et al. Modulation of human immune response by Echinococus granulosus antigen B and its possible role in evading host defenses. Infect Immun. 2001;69:288-96.
22. Margutti P, Ortona E, Vaccari S, Barca S, Rigano R, Teggi A, et al. Cloning and expression of a cDNA encoding an elongation factor 1β/δ protein from Echinococcus granulosus with immunogenic activity. Parasite Immunol. 1999;21:485-92.
23. Ortona E, Margutti P, Vaccari S, Rigano R, Profumo E, Buttari B, et al. Elongation factor 1β/δ of Echinococcus granulosus and allergic manifestations in human cystic echinococcosis. Clin Exp Immunol. 2001;125:110-6.
24. Ortona E, Vaccari S, Margutti P, Delunardo F, Rigano R, Profumo E, et al. Immunological characterization of Echinococcus granulosus cyclophilin, an allergen reactive with IgE and IgG4 from patient with cystic echinococcosis. Clin Exp Immunol. 2002;128:124-30.
25. Ortona E, Marguitti P, Delunardo F, Vaccari S, Rigano R, Profumo E, et al. Molecular and immunological characterization of the C-terminal region of a new Echinococcus granulosus Heat Shock Protein 70. Parasite Immunol. 2003;25:119-26.
26. Ortona E, Margutti P, Delunardo F, Nobili V, Profumo E, Rigano R, et al. Screening of an Echinococcus granulosus cDNA library with IgG4 from patient with cystic echinococcosis identifies a new tegumental protein involved in the immune escape. Clin Exp Immunol. 2005;142:528-38.
27. Delunardo F, Ortona E, Margutti P, Perdicchio M, Vacirca D, Teggi A, et al. Identification of a novel 19 kDa Echinococcus granulosus antigen. Acta Trop. 2010;113:42-7.
28. Gottstein B, Hemphill A. Echinococcus multilocularis: the parasite-host interplay. Exp Parasitol. 2008;119:447-52.
29. Balic A, Harcus Y, Holland MJ, Maizels RM. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol. 2004;34:3047-59.
30. Thomas PG, Varter MR, Atochina O, Da'Dara AA, Piskorska D, McGuire E, et al. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-depandent mechanism. J Immunol. 2003;171:5837-41.
31. Van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, et al. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J Biol Chem. 2002;277:48122-9.
32. MacDonald AS, Straw AD, Bauman B, Pearce EJ. CD8- dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol. 2001;167:1982-8.
33. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol. 2000;164:6453-60.
34. Elliott DE, Setiawan T, Metwali A, Blum A, Urban Jr JF, Weinstock JV. Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. Eur J Immunol. 2004;34:2690-8.
35. Zhou H, Sun X, Lv Z, Shen Y, Peng H, Yang L, et al. The secretions products from invading cercatiae of S. japonicum (0-3hRP) restrain mouse dendritic cells to mature. Parasitol Res. 2012;110:119-26.
36. Chen CC, Louie S, McCormick BA, Walker WA, Shi HN. Helminth-primed dendritic cells alter the host response to enteric bacterial infection. J Immunol. 2006;176:472-83.
37. Smits HH, de Jong EC, Wierenga EA, Kapsenberg ML. Different faces of regulatory DCs in homeostasis and immunity. Trends Immunol. 2005;26:123-9.
38. Mills KH. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol. 2004;4:841-55.
39. Hoerauf A, Brattig N. Resistance and susceptibility in human onchocerciasis - beyond Th1 vs Th2. Trends Parasitol. 2002;18:25-31.
40. + regulatory T cells. J Immunol. 2004;172:5986-93.
41. Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur J Immunol. 2007;37:1887-904.
42. + T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)-and Th2-inducing cytokines. J Exp Med. 2002;195:603-16.
43. Sundstedt A, O'Neill EJ, Nicolson KS, Wraith DC. Role for IL-10 in suppression mediated by peptide-induced regulatory T cells in vivo. J Immunol. 2003;170:1240-8.