Annelida: Recognition of Nonself in Earthworms
Earthworms belonging to oligochaete annelids became an important model for comparative immunologists in the early 1960s with the publication of transplantation experimental results reporting that autologous transplants of earthworm body wall pieces were accepted, but xenograft or even allografts were not. These transplantation experiments proved the existence of self or nonself recognition in earthworms, paving the way for extensive studies on the earthworm immune mechanisms that evolved to prevent the invasion of pathogens. In 1989 Charles Janeway, Jr., published a general concept based on the existence of pattern recognition receptors (PRRs) on the immune cells that recognize and bind conserved molecular structures of microorganisms known as pathogen-associated molecular patterns and thus trigger the immune response to potential pathogens. In the present review, the structure, specificity, and expression profile of PRRs characterized in earthworms are discussed and their role in innate defense suggested.
KeywordsAnnelids CCF Coelomic fluid Coelomocytes Earthworms Eisenia andrei Innate immunity LBP/BPI Pathogen-associated molecular patterns Pattern recognition receptors Recognition TLR Transplantation
This project has received funding from the European Union’s Horizon 2020 Research and Innovation Programme under the Marie Skłodowska-Curie grant agreement No. 671881. Special thanks to Miss Agáta Procházková for her help drawing a picture of an earthworm.
- Ashida M, Yamazaki IH (1990) In: Ohnishi E, Ishizaki H (eds) Biochemistry of the phenol oxidase system in insects: with special reference to its activation. Molting and metamorphosis. Japan Scientific Society Press, Tokyo, pp 239–265Google Scholar
- Beschin A, Bilej M, Hanssens F, Raymakers J, Van Dyck E, Revets H, Brys L, Gomez J, De Baetselier P, Timmermans M (1998) Identification and cloning of a glucan- and lipopolysaccharide-binding protein from Eisenia foetida earthworm involved in the activation of prophenoloxidase cascade. J Biol Chem 273(38):24948–24954CrossRefPubMedGoogle Scholar
- Cooper EL, Roch P (1994) In: Vetvicka V, Sima P, Cooper EL, Bilej M, Roch P (eds) Immunological profile of annelids: transplantation immunity. Immunology of Annelids. CRC Press, Boca Raton/Ann Arbor, pp 201–243Google Scholar
- Fontt OE, Beschin A, Van Dijck E, Vercruysse V, Bilej M, Lucas R, De Baetselier P, Vray B (2002) Trypanosoma cruzi is lysed by coelomic cytolytic factor-1, an invertebrate analogue of tumor necrosis factor, and induces phenoloxidase activity in the coelomic fluid of Eisenia foetida foetida. Dev Comp Immunol 26(1):27–34CrossRefGoogle Scholar
- Gonzalez M, Gueguen Y, Destoumieux-Garzon D, Romestand B, Fievet J, Pugniere M, Roquet F, Escoubas JM, Vandenbulcke F, Levy O, Saune L, Bulet P, Bachere E (2007) Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. Proc Natl Acad Sci U S A 104(45):17759–17764CrossRefPubMedPubMedCentralGoogle Scholar
- Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300(1):349–365CrossRefPubMedGoogle Scholar
- Kozhemyako VB, Rebrikov DV, Lukyanov SA, Bogdanova EA, Marin A, Mazur AK, Kovalchuk SN, Agafonova EV, Sova VV, Elyakova LA, Rasskazov VA (2004) Molecular cloning and characterization of an endo-1,3-beta-D-glucanase from the mollusk Spisula sachalinensis. Comp Biochem Physiol B Biochem Mol Biol 137(2):169–178CrossRefPubMedGoogle Scholar
- Paris-Palacios S, Mosleh YY, Almohamad M, Delahaut L, Conrad A, Arnoult F, Biagianti-Risbourg S (2010) Toxic effects and bioaccumulation of the herbicide isoproturon in Tubifex tubifex (Oligocheate, Tubificidae): a study of significance of autotomy and its utility as a biomarker. Aquat Toxicol 98(1):8–14CrossRefPubMedGoogle Scholar
- Seymour J, Nappi AJ, Valembois P (1992) Characterization of a phenoloxidase of the coelomic fluid of the earthworm Eisenia fetida andrei. Anim Biol 2:1–6Google Scholar
- Tasiemski A, Schikorski D, Le Marrec-Croq F, Camp CPV, Boidin-Wichlacz U, Sautiere PE (2007) Hedistin: a novel antimicrobial peptide containing bromotryptophan constitutively the marine annelid, expressed in the NK cells-like of Nereis diversicolor. Dev Comp Immunol 31(8):749–762CrossRefPubMedGoogle Scholar
- Valembois P (1971) Etude ultrastructurale des coelomocytes du lombricien Eisenia foetida Sav. Bull Soc Zool Fr 96:59–72Google Scholar