Giardia duodenalis stimulates partial maturation of bovine dendritic cells associated with altered cytokine secretion and induction of T-cell proliferation

Parasite Immunology

Volumn 36, Issue 4, 2014, Pages 157-169

  Grit, G H ^a   Devriendt, B ^a   Van Coppernolle, S ^a   Geurden, T ^a,c   Hope, J ^b   Vercruysse, J ^a   Cox, E ^a   Geldhof, P ^a   Claerebout, E ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Zoetis Veterinary Medicine Research and Development   (Belgium)

Author keywords

Cattle; Dendritic cells; Giardia duodenalis; Maturation; T cell proliferation

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OVALBUMIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CATTLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; GAMMA DELTA T LYMPHOCYTE; GENETIC TRANSCRIPTION; GIARDIA LAMBLIA; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MALE; MONOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TROPHOZOITE;

CATTLE; DENDRITIC CELLS; GIARDIA DUODENALIS; MATURATION; T-CELL PROLIFERATION;

ANIMALS; CATTLE; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; ENDOCYTOSIS; GIARDIA LAMBLIA; INTERLEUKIN-10; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MALE; OVALBUMIN; T-LYMPHOCYTE SUBSETS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84897708139     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12095     Document Type: Article

References (39)

1. Savioli L, Smith H & Thomson A. Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trends Parasitol 2006; 22: 203-208.
2. Geurden T, Vercruysse J & Claerebout E. Is Giardia a significant pathogen in production animals? Exp Parasitol 2010a; 124: 98-106.
3. Geurden T, Vandenhoute E, Pohle H, et al. The effect of a fenbendazole treatment on cyst excretion and weight gain in calves experimentally infected with Giardia duodenalis. Vet Parasitol 2010b; 169: 18-23.
4. Buret AG. Mechanisms of epithelial dysfunction in giardiasis. Gut 2007; 56: 316-317.
5. Robertson LJ, Hanevik K, Escobedo AA, Morch K & Langeland N. Giardiasis- why do the symptoms sometimes never stop? Trends Parasitol 2010; 26: 75-82.
6. Gottstein B, Harriman GR, Conrad JT & Nash TE. Antigenic variation in Giardia lamblia: cellular and humoral immune response in a mouse model. Parasite Immunol 1990; 12: 659-673.
7. Roxtröm-Lindquist K, Palm D, Reiner D, Ringqvist E & Svärd G. Giardia immunity - an update. Trends Parasitol 2006; 22: 26-31.
8. Scott KGE, Yu LCH & Buret AG. Role of CD8+ and CD4+ T Lymphocytes in jejunal mucosal injury during murine giardiasis. Infect Immun 2004; 72: 3536-3542.
9. Singer SM & Nash TE. T-cell-dependent control of acute Giardia lamblia infections in mice. Infect Immun 2000; 68: 170-175.
10. Zhou P, Li E, Shea-Donohue T & Singer SM. Tumor necrosis factor alpha contributes to protection against Giardia lamblia infection in mice. Parasite Immunol 2007; 29: 367-374.
11. Dreesen L, Rinaldi M, Chiers K, et al. Microarray analysis of the intestinal host response in Giardia duodenalis assemblage E infected calves. PLoS ONE 2012; 7: e40985.
12. Taminnelli V, Ecker J, Sydler T, Gottstein B, Corboz L & Hofmann M. Experimental infection of calves and sheep with bovine Giardia isolates. Schweiz Arch Tierheilkd 1998; 131: 551-564.
13. Ruest N, Couture Y, Faubert GM & Girard C. Morphological changes in the jejunum of calves naturally infected with Giardia spp. and Cryptosporidium spp. Vet Parasitol 1997; 69: 177-186.
14. Roxtröm-Lindquist K, Ringqvist E, Palm D & Svärd S. Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect Immun 2005; 73: 8204-8208.
15. Terrazas CA, Terrazas LI & Gomez-Garcia L. Modulation of dendritic cell responses by parasites: a common strategy to survive. J Biomed Biotechnol 2010; Article ID 357106, doi:10.1155/2010/357106.
16. Oberhuber G, Kaster N & Stolte M. Giardiasis, a histologic analysis of 567 cases. Scand J Gastroenterol 1997; 32: 48-51.
17. Kamda JD & Singer SM. Phosphoinositide 3-kinase-dependent inhibition of dendritic cell interleukin-12 production by Giardia lamblia. Infect Immun 2009; 77: 685-693.
18. Keister DB. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 1983; 77: 487-488.
19. Hope JC, Whelan AO, Hewinson RG, Vordemeier M & Howard CJ. Maturation of bovine dendritic cells by lipopeptides. Vet Immunol Immunopathol 2003; 95: 21-31.
20. Werling D, Hope JC, Chaplin P, Collins RA, Taylor G & Howard CJ. Involvement of caveolae in the uptake of respiratory syncytial virus antigen by dendritic cells. J Leukoc Biol 1999; 66: 50-58.
21. Inumaru S, Kohuho T, Denham S, et al. Expression of biologically active recombinant porcine GM-CSF by baculovirus gene expression system. Immunol Cell Biol 1998; 76: 195-201.
22. Ardeshna KM, Pizzey AR, Devereux S & Khwaja A. The PI3 kinase, p38 SAP kinase and NF-κB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 2000; 96: 1039-1046.
23. Hope JC, Kwong LS, Thom M, et al. Development of detection methods for ruminant interleukin (IL)-4. J Immunol Methods 2005; 301: 114-123.
24. Kwong LS, Hope JC, Thom ML, et al. Development of an ELISA for bovine IL-10. Vet Immunol Immunopathol 2002; 85: 213-223.
25. Hope JC, Kwong LS, Entrican G, Watttegedera S, Bembridge GP & Howard CJ. Development of detection methods for ruminant interleukin (IL)-12. Vet Immunol Immunopathol 2002; 85: 213-223.
26. Schreiner B, Mitsdoerffer M, Kieseier BC, et al. Interferon-β enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis. J Neuroimmunol 2004; 155: 172-182.
27. Atay S, Villlard M, Martin M, Parnell S, Kosiewicz M & Alard P. Relationship between the high expression of nuclear beta-catenin in dendritic cells from NOD mice and the pro-inflammatory phenotype of these cells. J Immunol 2009; 182: 99.18.
28. 3. Blood 2005; 106: 3490-3497.
29. Kapsenberg LM. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 2003; 3: 984-993.
30. Geurden T, Geldhof P, Levecke B, et al. Mixed Giardia duodenalis assemblage A and E infections in calves. Int J Parasitol 2008; 38: 259-264.
31. Galli SJ, Nakae S & Tsai M. Mast cells in the development of adaptive immune responses. Nat Immun 2005; 6: 135-142.
32. Zhou P, Li E, Zhu N, Robertson J, Nash T & Singer SM. Role of interleukin-6 in the control of acute and chronic Giardia lamblia infections in mice. Infect Immun 2003; 71: 1556-1568.
33. Tan JKH & O'Neill HC. Maturation requirements for dendritic cells in T cell stimulation leading to tolerance versus immunity. J Leukoc Biol 2005; 78: 319-324.
34. Cools N, Ponsaerts P, Van Tendeloo VFI & Berneman ZN. Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J Leukoc Biol 2007; 82: 1365-1374.
35. Shortman K & Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007; 7: 19-30.
36. Werling D, Collins RA, Taylor G & Howard CJ. Cytokine responses of bovine dendritic cells and T-cells following exposure to live or inactivated bovine respiratoir syncytial virus. J Leukoc Biol 2002; 72: 297-304.
37. Hanevik K, Kristoffersen E, Svard S, et al. Human cellular immune response against Giardia lamblia 5 years after acute giardiasis. J Infect Dis 2011; 204: 1779-1789.
38. Ebert EC. Giardia induces proliferation and interferon γ production by intestinal lymphocytes. Gut 1999; 44: 342-346.
39. + T cells act as immune regulatory cells ex vivo. Vet Res 2009; 40: 6.