Helminth-derived immunomodulators: Can understanding the worm produce the pill?

Nature Reviews Immunology

Volumn 10, Issue 4, 2010, Pages 278-284

  Harnett, William ^a   Harnett, Margaret M ^b  

^a UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; CATHEPSIN; CYSTATIN; CYSTEINE PROTEINASE; DOUBLE STRANDED RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOMODULATING AGENT; LYSOPHOSPHATIDYLSERINE; MITOGEN ACTIVATED PROTEIN KINASE; PEROXIREDOXIN; PHOSPHATIDYLSERINE; TOLL LIKE RECEPTOR;

ALLERGIC DISEASE; AUTOIMMUNE DISEASE; HELMINTH; HOST PARASITE INTERACTION; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATORY DISEASE; NONHUMAN; NOTE; PRIORITY JOURNAL;

ANIMALS; HELMINTH PROTEINS; HELMINTHIASIS; HUMANS; HYPERSENSITIVITY; IMMUNOLOGIC FACTORS;

EID: 77950083594     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2730     Document Type: Note

References (77)

1. de Silva, N. R. et al. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 19, 547-551 (2003).
2. Ruyssers, N. E. et al. Worms and the treatment of inflammatory bowel disease: are molecules the answer? Clin. Dev. Immunol. 2008, 567314-567320 (2008).
3. Cooper, P. J. Interactions between helminth parasites and allergy. Curr. Opin. Allergy Clin. Immunol. 9, 29-37 (2009).
4. van Riet, E., Hartgers, F. C. & Yazdanbakhsh, M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 212, 475-490 (2007)
5. Maizels, R. M. Infections and allergy \ helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 17, 656-661 (2005).
6. Carvalho, L. et al. Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126, 28-34 (2009).
7. Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr, Stadecker, M. J. & Gause, W. C. Protective immune mechanisms in helminth infection. Nature Rev. Immunol. 7, 975-987 (2007).
8. David, T., Thomas, C., Zaccone, P., Dunne, D. W. & Cooke, A. The impact of infection on the incidence of autoimmune disease. Curr. Top. Med. Chem. 4, 521-529 (2004).
9. Cooke, A. Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126, 12-17 (2009).
10. Harnett, W. & Harnett, M. M. Therapeutic immunomodulators from nematode parasites. Expert Rev. Mol. Med. 10, e18 (2008).
11. H2-type allergic reactions by helminth infection. Nature Rev. Immunol. 7, 220-230 (2007).
12. Helmby, H. Helminths and our immune system: friend or foe? Parasitol. Int. 58, 121-127 (2009).
13. Erb, K. J. Can helminths or helminth-derived products be used in humans to prevent or treat allergic diseases? Trends Immunol. 30, 75-82 (2009).
14. Elliott, D. E., Summers, R. W. & Weinstock, J. V. Helminths as governors of immune-mediated inflammation. Int. J. Parasitol. 37, 457-464 (2007).
15. van der Kleij, D. et al. A novel host-parasite lipid crosstalk. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129 (2002).
16. Harn, D. A., McDonald, J., Atochina, O. & Da'dara, A. A. Modulation of host immune responses by helminth glycans. Immunol. Rev. 230, 247-257 (2009).
17. Aksoy, E. et al. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 280, 277-283 (2005).
18. Vanhoutte, F. et al. Toll-like receptor (TLR)2 and TLR3 sensing is required for dendritic cell activation, but dispensable to control Schistosoma mansoni infection and pathology. Microbes Infect. 9, 1606-1613 (2007).
19. van Riet, E. et al. Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol. 10, 9 (2009).
20. Goodridge, H. S. et al. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J. Immunol. 174, 284-293 (2005).
21. Melendez, A. J. et al. Inhibition of FcεRI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nature Med. 13, 1375-1381 (2007).
22. Donnelly, S. et al. Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J. 22, 4022-4032 (2008).
23. Atochina, O. & Harn, D. Prevention of psoriasis-like lesions development in fsn/fsn mice by helminth glycans. Exp. Dermatol. 15, 461-468 (2006).
24. Thomas, P. G. et al. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171, 5837-5841 (2003).
25. Van Liempt, E. et al. Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and Schistosoma mansoni egg antigens. J. Biol. Chem. 279, 33161-33167 (2004).
26. van Liempt, E. et al. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol. Immunol. 44, 2605-2615 (2007).
27. Kane, C. M., Jung, E. & Pearce, E. J. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect. Immun. 76, 5754-5759 (2008).
28. Goodridge, H. S., Deehan, M. R., Harnett, W. & Harnett, M. M. Subversion of immunological signalling by a filarial nematode phosphorylcholine-containing secreted product. Cell Signal. 17, 11-16 (2005).
29. Goodridge, H. S., Stepek, G., Harnett, W. & Harnett, M. M. Signalling mechanisms underlying subversion of the immune response by the filarial nematode secreted product ES-62. Immunology 11 5, 296-304 (2005).
30. Harnett, M. M., Melendez, A. J. & Harnett, W. The therapeutic potential of the filarial nematode-derived immunomodulator, ES-62, in inflammatory disease. Clin. Exp. Immunol. 159, 256-267 (2010).
31. Harnett, M. M. et al. The phosphorycholine moiety of the filarial nematode immunomodulator ES-62 is responsible for its anti-inflammatory action in arthritis. Ann. Rheum. Dis. 67, 518-523 (2008).
32. McInnes, I. B. et al. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J. Immunol. 171, 2127-2133 (2003).
33. Rigano, R. et al. Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infect. Immun. 75, 1667-1678 (2007).
34. Kean, D. E. et al. Dissecting Ascaris glycosphingolipids for immunomodulatory moieties \ the use of synthetic structural glycosphingolipid analogues. Parasite Immunol. 28, 69-76 (2006).
35. Deehan, M. R. et al. Immunomodulatory properties of Ascaris suum glycosphingolipids \ phosphorylcholine and non-phosphorylcholine-dependent effects. Parasite Immunol. 24, 463-469 (2002).
36. Brannstrom, K., Sellin, M. E., Holmfeldt, P., Brattsand, M. & Gullberg, M. The Schistosoma mansoni protein Sm16/SmSLP/SmSPO-1 assembles into a nine-subunit oligomer with potential To inhibit Toll-like receptor signaling. Infect. Immun. 77, 1144-1154 (2009).
37. Donnelly, S. et al. Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3. J. Biol. Chem. 285, 3383-3392 (2010).
38. Kanzler, H., Barrat, F. J., Hessel, E. M. & Coffman, R. L. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nature Med. 13, 552-559 (2007).
39. Trinchieri, G. & Sher, A. Cooperation of Toll-like receptor signals in innate immune defence. Nature Rev. Immunol. 7, 179-190 (2007).
40. O'Neill, L. A. & Bowie, A. G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nature Rev. Immunol. 7, 353-364 (2007).
41. Goodridge, H. S. et al. Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunol. 29, 127-137 (2007).
42. Thomas, P. G., Carter, M. R., Da'dara, A. A., Desimone, T. M. & Harn, D. A. A helminth glycan induces APC maturation via alternative NF-κB activation independent of IκBα degradation. J. Immunol. 175, 2082-2090 (2005).
43. Agrawal, S. et al. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171, 4984-4989 (2003).
44. Dillon, S. et al. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J. Immunol. 172, 4733-4743 (2004).
45. Goodridge, H. S., Harnett, W., Liew, F. Y. & Harnett, M. M. Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and-independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology 109, 415-425 (2003).
46. Kane, C. M. et al. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173, 7454-7461 (2004).
47. Breuilh, L. et al. Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells. Infect. Immun. 75, 5148-5157 (2007).
48. Dillon, S. et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928 (2006).
49. Kubo-Murai, M. et al. Protein kinase C5 binds TIRAP/ Mal to participate in TLR signaling. Mol. Immunol. 44, 2257-2264 (2007).
50. Lai, W. Q. et al. The role of sphingosine kinase in a murine model of allergic asthma. J. Immunol. 180, 4323-4329 (2008).
51. Lai, W. Q. et al. Distinct roles of sphingosine kinase 1 and 2 in murine collagen-induced arthritis. J. Immunol. 183, 2097-2103 (2009).
52. Pushparaj, P. N. et al. Sphingosine kinase 1 is pivotal for FcsRI-mediated mast cell signaling and functional responses in vitro and in vivo. J. Immunol. 183, 22 1-227 (2009).
53. Watts, C. Location, location, location: identifying the neighborhoods of LPS signaling. Nature Immunol. 9, 343-345 (2008).
54. Kagan, J. C. et al. TRAM couples endocytosis of Tolllike receptor 4 to the induction of interferon-p. Nature Immunol. 9, 361-368 (2008).
55. Halaas, O., Husebye, H. & Espevik, T. The journey of Toll-like receptors in the cell. Adv. Exp. Med. Biol. 598, 35-48 (2007).
56. Husebye, H. et al. Endocytic pathways regulate Tolllike receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25, 683-692 (2006).
57. Kutuzova, G. D., Albrecht, R. M., Erickson, C. M. & Qureshi, N. Diphosphoryl lipid A from Rhodobacter sphaeroides blocks the binding and internalization of lipopolysaccharide in RAW 264.7 cells. J. Immunol. 167, 482-489 (2001).
58. Szabo, G., Dolganiuc, A., Dai, Q. & Pruett, S. B. TLR4, ethanol, and lipid rafts: a new mechanism of ethanol action with implications for other receptor-mediated effects. J. Immunol. 178, 1243-1249 (2007).
59. Grange, P. A. et al. Production of superoxide anions by keratinocytes initiates P. acnes-induced inflammation of the skin. PLoS Pathog. 5, e1000527 (2009).
60. Cervi, L., MacDonald, A. S., Kane, C, Dzierszinski, F & Pearce, E. J. Cutting edge: dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th 1 and helminth-specific Th2 responses. J. Immunol. 172, 2016-2020 (2004).
61. Geiss-Friedlander, R. & Melchior, F. Concepts in sumoylation: a decade on. Nature Rev. Mol. Cell Biol. 8, 947-956 (2007).
62. Lin, A. E. & Mak, T W The role of E3 ligases in autoimmunity and the regulation of autoreactive T cells. Curr. Opin. Immunol. 19, 665-673 (2007).
63. Semnani, R. T. et al. Inhibition of TLR3 and TLR4 function and expression in human dendritic cells by helminth parasites. Blood 112, 1290-1298 (2008).
64. Babu, S., Blauvelt, C. P., Kumaraswami, V. & Nutman, T. B. Regulatory networks induced by live parasites impair both Th1 and Th2 pathways in patent lymphatic filariasis: implications for parasite persistence. J. Immunol. 176, 3248-3256 (2006).
65. Taylor, J. J., Krawczyk, C. M., Mohrs, M. & Pearce, E. J. Th2 cell hyporesponsiveness during chronic murine schistosomiasis is cell intrinsic and linked to GRAIL expression. J. Clin. Invest. 11 9, 1019-1028 (2009).
66. Bachmaier, K. et al. E3 ubiquitin ligase Cblb regulates the acute inflammatory response underlying lung injury. Nature Med. 13, 920-926 (2007).
67. Qu, X. et al. Negative regulation of FcεRI-mediated mast cell activation by a ubiquitin-protein ligase Cbl-b. Blood 103, 1779-1786 (2004).
68. Hartmann, S. & Lucius, R. Modulation of host immune responses by nematode cystatins. Int. J. Parasitol. 33, 1291-1302 (2003).
69. Schnoeller, C. et al. A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J. Immunol. 180, 4265-4272 (2008).
70. Rzepecka, J. et al. Calreticulin from the intestinal nematode Heligmosomoides polygyrus is a Th2-skewing protein and interacts with murine scavenger receptor-A. Mol. Immunol. 46, 1109-1119 (2009).
71. Imai, S. & Fujita, K. Molecules of parasites as immunomodulatory drugs. Curr. Top. Med. Chem. 4, 539-552 (2004).
72. Schramm, G. et al. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J. Immunol. 178, 6023-6027 (2007).
73. Steinfelder, S. et al. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206, 1681-1690 (2009).
74. H2 cytokine-dependent immunity. Nature Immunol. 10, 697-705 (2009).
75. Everts, B. et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 206, 1673-1680 (2009).
76. Smith, P. et al. Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity. J. Exp. Med. 202, 1319-1325 (2005).
77. Roelofs, M. F., Abdollahi-Roodsaz, S., Joosten, L. A., van den Berg, W. B. & Radstake, T. R. The orchestra of Toll-like receptors and their potential role in frequently occurring rheumatic conditions. Arthritis Rheum. 58, 338-348 (2008).