Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 49, 2010, Pages 21087-21092

  Hanington, Patrick C ^a   Forys, Michelle A ^a   Dragoo, Jerry W ^a   Zhang, Si Ming ^a   Adema, Coen M ^a   Loker, Eric S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Evolution; Host parasite interactions; Immunology; Parasitology; Schistosomiasis

Indexed keywords

FIBRINOGEN RELATED PROTEIN 3; LECTIN; OPSONIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMPHALARIA GLABRATA; CONTROLLED STUDY; ECHINOSTOMA; ECHINOSTOMIASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

ADAPTIVE IMMUNITY; ANIMALS; BIOMPHALARIA; ECHINOSTOMA; ECHINOSTOMIASIS; IMMUNOGLOBULINS; LECTINS; OPSONIN PROTEINS; PHAGOCYTOSIS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI;

BIOMPHALARIA GLABRATA; ECHINOSTOMA PARAENSEI; GASTROPODA; INVERTEBRATA; SCHISTOSOMA MANSONI; TREMATODA; VERTEBRATA;

EID: 78650424339     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1011242107     Document Type: Article

References (45)

1. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323-329.
2. Alper S, McBride SJ, Lackford B, Freedman JH, Schwartz DA (2007) Specificity and complexity of the Caenorhabditis elegans innate immune response. Mol Cell Biol 27: 5544-5553.
3. Zhang SM, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305:251-254.
4. Watson FL, et al. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309:1874-1878.
5. Rast JP, Smith LC, Loza-Coll M, Hibino T, Litman GW (2006) Genomic insights into the immune system of the sea urchin. Science 314:952-956. (Pubitemid 44749931)
6. Guo P, et al. (2009) Dual nature of the adaptive immune system in lampreys. Nature 459:796-801.
7. Buckley KM, Terwilliger DP, Smith LC (2008) Sequence variations in 185/333 messages from the purple sea urchin suggest posttranscriptional modifications to increase immune diversity. J Immunol 181:8585-8594.
8. Litman GW, Dishaw LJ, Cannon JP, Haire RN, Rast JP (2007) Alternative mechanisms of immune receptor diversity. Curr Opin Immunol 19:526-534.
9. Little TJ, Hultmark D, Read AF (2005) Invertebrate immunity and the limits of mechanistic immunology. Nat Immunol 6:651-654.
10. Kurtz J (2005) Specific memory within innate immune systems. Trends Immunol 26: 186-192.
11. Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: Potential for coevolution and frequency-dependent selection. Evolution 55: 1136-1145.
12. Lie KJ, Heyneman D (1979) Acquired resistance to echinostomes in four Biomphalaria glabrata strains. Int J Parasitol 9:533-537.
13. Schmid-Hempel P, Puhr K, Kruger N, Reber C, Schmid-Hempel R (1999) Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53:426-434.
14. Hauton C, Smith VJ (2007) Adaptive immunity in invertebrates: A straw house without a mechanistic foundation. Bioessays 29:1138-1146.
15. Adema CM, Hertel LA, Miller RD, Loker ES (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 94:8691-8696.
16. Brooker S, et al. (2009) An updated atlas of human helminth infections: The example of East Africa. Int J Health Geogr 8:42.
17. Chitsulo L, Loverde P, Engels D (2004) Schistosomiasis. Nat Rev Microbiol 2:12-13.
18. Cribb TH, Bray RA, Olson PD, Littlewood DT (2003) Life cycle evolution in the digenea: A new perspective from phylogeny. Adv Parasitol 54:197-254.
19. Lockyer AE, Jones CS, Noble LR, Rollinson D (2004) Trematodes and snails: An intimate association. Can J Zool 82:251-269.
20. Adema CM, et al. (2010) Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 47: 849-860.
21. Hanington PC, Lun CM, Adema CM, Loker ES (2010) Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. Int J Parasitol 40:819-831.
22. Wu XJ, et al. (2009) Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol Biochem Parasitol 164: 32-44.
23. Bayne CJ (2009) Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: A 2009 assessment. Mol Biochem Parasitol 165:8-18.
24. Miller AN, Raghavan N, FitzGerald PC, Lewis FA, Knight M (2001) Differential gene expression in haemocytes of the snail Biomphalaria glabrata: Effects of Schistosoma mansoni infection. Int J Parasitol 31:687-696.
25. Loker ES, Cimino DF, Stryker GA, Hertel LA (1987) The effect of size of M line Biomphalaria glabrata on the course of development of Echinostoma paraensei. J Parasitol 73:1090-1098.
26. Chen JM, Cooper DN, Chuzhanova N, Férec C, Patrinos GP (2007) Gene conversion: Mechanisms, evolution and human disease. Nat Rev Genet 8:762-775.
27. Zhang SM, Loker ES (2004) Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 341:255-266.
28. Mounkassa JB, Jourdane J (1990) Dynamics of the leukocytic response of Biomphalaria glabrata during the larval development of Schistosoma mansoni and Echinostoma liei. J Invertebr Pathol 55:306-311.
29. Peterson NA, Hokke CH, Deelder AM, Yoshino TP (2009) Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: Differential expression during the miracidium-to-sporocyst transformation. Int J Parasitol 39:1331-1344.
30. Kvennefors EC, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32:1582-1592.
31. Gruden-Movsesijan A, Milosavljevic LjS (2006) The involvement of the macrophage mannose receptor in the innate immune response to infection with parasite Trichinella spiralis. Vet Immunol Immunopathol 109:57-67.
32. Kawabata S, Tsuda R (2002) Molecular basis of non-self recognition by the horseshoe crab tachylectins. Biochim Biophys Acta 1572:414-421. (Pubitemid 35246358)
33. Ataev GL, Coustau C (1999) Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility/ resistance. Dev Comp Immunol 23:187-198.
34. Jiang Y, Loker ES, Zhang SM (2006) In vivo and in vitro knockdown of FREP2 gene expression in the snail Biomphalaria glabrata using RNA interference. Dev Comp Immunol 30:855-866.
35. Hertel LA, Adema CM, Loker ES (2005) Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 29:295-303.
36. Zhang SM, Zeng Y, Loker ES (2008) Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun 14:175-189.
37. Loker ES, Adema CM, Zhang SM, Kepler TB (2004) Invertebrate immune systems-not homogeneous, not simple, not well understood. Immunol Rev 198:10-24.
38. Zhang H, et al. (2009) A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor. Fish Shellfish Immunol 26:56-64.
39. Middha S, Wang X (2008) Evolution and potential function of fibrinogen-like domains across twelve Drosophila species. BMC Genomics 9:260.
40. Moné Y, et al. (2010) A large repertoire of parasite epitopesmatched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 4.
41. Dong Y, Taylor HE, Dimopoulos G (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4:e229.
42. Litman GW, Cannon JP, Rast JP (2005) New insights into alternative mechanisms of immune receptor diversification. Adv Immunol 87:209-236.
43. Kurtz J, Armitage SA (2006) Alternative adaptive immunity in invertebrates. Trends Immunol 27:493-496.
44. Cooper MD, Alder MN (2006) The evolution of adaptive immune systems. Cell 124: 815-822.
45. Tusher V, Tibshirani R, Chu C (2001) Significance analysis of microarrays applied to ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.