Abstract
The coelomic cavity is part of the main body plan of annelids. This fluid filled space takes up a considerable volume of the body and serves as an important site of exchange of both metabolites and proteins. In addition to low molecular substances such as amino acids and glucose and lactate, the coelomic fluid contains different proteins that can arise through release from adjacent tissues (intestine) or from secretion by coelomic cells. In this chapter, we will review the current knowledge about the proteins in the annelid coelomic fluid. Given the number of more than 20,000 extant annelid species, existing studies are confined to a relatively few species. Most studies on the oligochaetes are confined to the earthworms—clearly because of their important role in soil biology. In the polychaetes (which might represent a paraphyletic group) on the other hand, studies have focused on a few species of the Nereidid family. The proteins present in the coelomic fluid serve different functions and these have been studied in different taxonomic groups. In oligochaetes, proteins involved antibacterial defense such as lysenin and fetidin have received much attention in past and ongoing studies. In polychaetes, in contrast, proteins involved in vitellogenesis and reproduction, and the vitellogenic function of coelomic cells have been investigated in more detail. The metal binding metallothioneins as well as antimicrobial peptides, have been investigated in both oligochaetes and polychaetes. In the light of the literature available, this review will focus on lipoproteins, especially vitellogenin, and proteins involved in defense reactions. Other annelid groups such as the Pogonophora, Echiura, and Sipuncula (now considered polychaetes), have not received much attention and therefore, this overview is far from being complete.
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References
Altincicek B, Vilcinskas A (2007) Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii. Front Zool 4:18. https://doi.org/10.1186/1742-9994-4-18
Andrä J, Jakovkin I, Grötzinger J, Hecht O, Krasnosdembskaya AD, Goldmann T, Gutsmann T, Leippe M (2008) Structure and mode of action of the antimicrobial peptide arenicin. Biochem J 410(1):113–122
Arosio P, Levi S, Gabri E, Stefanini S, Finazziagro A, Chiancone E (1984) Properties of ferritin from the earthworm Octolasium complanatum. Biochim Biophys Acta 787(3):264–269. https://doi.org/10.1016/0167-4838(84)90318-2
Baert JL (1985) Multiple forms of vitellin in young oocytes of Perinereis cultrifera (Polychaete Annelid): occurrence and relation to vitellin maturation in the oocyte. Comp Biochem Physiol 81B:851–856. https://doi.org/10.1016/0305-0491(85)90078-1
Baert JL (1986) Evidence for vitellin maturation within the oocytes of Perinereis cultrifera (Polychaete Annelid). Comp Biochem Physiol 83B:847–853. https://doi.org/10.1016/0305-0491(86)90159-8
Baert JL, Slomianny MC (1987) Heterosynthetic origin of the major yolk protein, vitellin, in a nereid, Perinereis cultrifera (Polychaete annelid). Comp Biochem Physiol 88B:1191–1199. https://doi.org/10.1016/0305-0491(87)90023-X
Baert JL, Slomianny MC (1992) Vitellin accumulation and vitellogenin synthesis in relation to oogenesis in Perinereis cultrifera (Polychaeta, Annelida). Invertebr Reprod Dev 21:121–128. https://doi.org/10.1080/07924259.1992.9672228
Baert JL, Britel M, Slomianny MC, Delbart C, Fournet B, Sautiere P, Malecha J (1991) Yolk protein in leech. Identification, purification and characterization of vitellin and vitellogenin. Eur J Biochem 201 (1):191–198. https://doi.org/10.1111/j.1432-1033.1991.tb16273.x
Baert JL, Britel M, Sautiere P, Malecha J (1992) Ovohemerythrin, a major 14-kDa yolk protein distinct from vitellogenin in leech. Eur J Biochem 209(2):563–569. https://doi.org/10.1111/j.1432-1033.1992.tb17321.x
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):24948–24954. https://doi.org/10.1074/jbc.273.38.24948
Bilej M, Brys L, Beschin A, Lucas R, Vercauteren E, Hanušová R, De Baetselier P (1995) Identification of a cytolytic protein in the coelomic fluid of Eisenia foetida earthworms. Immunol Let 45:123–128
Bodo K, Boros A, Rumpler E, Molnar L, Borocz K, Nemeth P, Engelmann P (2019) Identification of novel lumbricin homologues in Eisenia andrei earthworms. Dev Comp Immunol 90:41–46. https://doi.org/10.1016/j.dci.2018.09.001
Bokori-Brown M, Martin TG, Naylor CE, Basak AK, Titball RW, Savva CG (2016) Cryo-EM structure of lysenin pore elucidates membrane insertion by an aerolysin family protein. Nat Commun 7:11293. https://doi.org/10.1038/ncomms11293
Bonnier P, Baert J-L (1992) Vitellogenesis in the sand worm, Nereis diversicolor. Comp Biochem Physiol B 102(5):785–790. https://doi.org/10.1016/0305-0491(92)90080-B
Bruhn H, Winkelmann J, Andersen C, Andra J, Leippe M (2006) Dissection of the mechanisms of cytolytic and antibacterial activity of lysenin, a defence protein of the annelid Eisenia fetida. Dev Comp Immunol 30(7):597–606. https://doi.org/10.1016/j.dci.2005.09.002
Bruno R, Maresca M, Canaan S, Cavalier JF, Mabrouk K, Boidin-Wichlacz C, Olleik H, Zeppilli D, Brodin P, Massol F, Jollivet D, Jung S, Tasiemski A (2019) Worms' antimicrobial peptides. Mar Drugs 17(9). https://doi.org/10.3390/md17090512
Calisi A, Lionetto MG, De Lorenzis E, Leomanni A, Schettino T (2014) Metallothionein induction in the coelomic fluid of the earthworm Lumbricus terrestris following heavy metal exposure: a short report. Biomed Res Int 2014:109386. https://doi.org/10.1155/2014/109386
Chino H, Downer RG, Takahashi K (1977) The role of diacylglycerol-carrying lipoprotein I in lipid transport during insect vitellogenesis. Biochim Biophys Acta 487(3):508–516. https://doi.org/10.1016/0005-2760(77)90220-x
Cho JH, Park CB, Yoon YG, Kim SC (1998) Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA cloning and molecular characterization. Biochim Biophys Acta 1408(1):67–76. https://doi.org/10.1016/s0925-4439(98)00058-1
Claus H, Decker H (2006) Bacterial tyrosinases. Syst Appl Microbiol 29:3–14. https://doi.org/10.1016/j.syapm.2005.07.012
Coates CJ, Decker H (2017) Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin. Cell Mol Life Sci 74(2):293–317. https://doi.org/10.1007/s00018-016-2326-7
Cooper EL (2002) Invertebrate immune responses. In: Advances in comparative and environmental physiology, vol 23. Springer, Berlin. https://doi.org/10.1007/978-3-642-79693-7
Cooper EL, Stein EA (1981) Oligochaetes. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New York, pp 76–140
Cooper EL, Kauschke E, Cossarizza A (2001) Annelid humoral immunity: cell lysis in earthworms. In: Beck G, Sugumaran M, Cooper EL (eds) Phylogenetic perspectives on the vertebrate immune system. Adv. Exp. Med. Biol. Springer, Berlin,
Costa-Paiva EM, Schrago CG, Halanych KM (2017) Broad phylogenetic occurrence of the oxygen-binding hemerythrins in bilaterians. Genome Biol Evol 9(10):2580–2591. https://doi.org/10.1093/gbe/evx181
Costa-Paiva EM, Schrago CG, Coates CJ, Halanych KM (2018) Discovery of novel hemocyanin-like genes in metazoans. Biol Bull 235:134–151. https://doi.org/10.1086/700181
Çotuk A, Dales RP (1984) Lysozyme activity in the coelomic fluid and coelomocytes of the earthworm Eisenia foetida Sav. in relation to bacterial infection. Comp Biochem Physiol A 78:469–474. https://doi.org/10.1016/0300-9629(84)90580-2
Dales RP, Dixon LJR (1980) Responses of polychaete annelids to bacterial infection. Comp Biochem Physiol A 67:391–396. https://doi.org/10.1016/S0300-9629(80)80014-4
Dales RP, Dixon RJ (1981) Polychaetes. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New York, pp 35–74
de Eguileor M, Grimaldi A, Tettamanti G, Valvassori R, Cooper EL, Lanzavecchia G (2000) Lipopolysaccharide-dependent induction of leech leukocytes that cross-react with vertebrate cellular differentiation markers. Tissue Cell 32(5):437–445
Decker H, Rimke T (1998) Tarantula hemocyanin shows phenoloxidase activity. J Biol Chem 273(40):25889–25892. https://doi.org/10.1074/jbc.273.40.25889
Deloffre L, Salzet B, Vieau D, Andries JC, Salzet M (2003) Antibacterial properties of hemerythrin of the sand worm Nereis diversicolor. Neuro Endocrinol Lett 24(1–2):39–45
Demuynck S, Sautiere P, van Beeumen J, Dhainaut-Courtois N (1991) Homologies between hemerythrins of sipunculids and cadmium-binding metalloprotein (MP II) from a polychaete annelid, Nereis diversicolor. C R Acad Sci III 312(7):317–322
Demuynck S, Li KW, Van der Schors R, Dhainaut-Courtois N (1993) Amino acid sequence of the small cadmium-binding protein (MP II) from Nereis diversicolor (annelida, polychaeta). Evidence for a myohemerythrin structure. Eur J Biochem 217 (1):151–156. https://doi.org/10.1111/j.1432-1033.1993.tb18230.x
Dhainaut A, Porchet-Henneré E (1988) Haemocytes and coelomocytes. In: Westheide W, Hermans CO (eds) Microfauna marina, vol 4. Gustav Fischer Verlag, Stuttgart, pp 216–230
Dhainaut A, Raveillon B, Mberi M, Porchet-Henneré E, Demuynck S (1989) Purification of an antibacterial protein in the coelomic fluid of Nereis diversicolor (Annelida, Polychaeta)—similitude with a cadmium-binding protein. Comp Biochem Phys C 94(2):555–560. https://doi.org/10.1016/0742-8413(89)90112-6
Eckelbarger KJ (2005) Oogenesis and oocytes. Hydrobiologia 535:179–198. https://doi.org/10.1007/s10750-004-4397-y
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340
Engelmann P, Palinkas L, Cooper EL, Nemeth P (2005) Monoclonal antibodies identify four distinct annelid leukocyte markers. Dev Comp Immunol 29(7):599–614. https://doi.org/10.1016/j.dci.2004.10.008
Fiołka MJ, Zagaja MP, Hułas-Stasiak M, Wielbo J (2012) Activity and immunodetection of lysozyme in earthworm Dendrobaena veneta (Annelida). J Invertebr Pathol 109:83–90. https://doi.org/10.1016/j.jip.2011.10.002
Fiołka MJ, Czaplewska P, Macur K, Buchwald T, Kutkowska J, Paduch R, Kaczynski Z, Wydrych J, Urbanik-Sypniewska T (2019a) Anti-Candida albicans effect of the protein-carbohydrate fraction obtained from the coelomic fluid of earthworm Dendrobaena veneta. PLoS ONE 14(3):e0212869. https://doi.org/10.1371/journal.pone.0212869
Fiołka MJ, Rzymowska J, Bilska S, Lewtak K, Dmoszynska-Graniczka M, Grzywnowicz K, Kazmierski W, Urbanik-Sypniewska T (2019b) Antitumor activity and apoptotic action of coelomic fluid from the earthworm Dendrobaena veneta against A549 human lung cancer cells. APMIS 127(6):435–448. https://doi.org/10.1111/apm.12941
Fischer A (1979) A vitellin-like antigen in the coelomic fluid of maturing Nereis virens females. Naturwissenschaften 66:316
Fischer A, Rabien H, Heacox AE (1991) Specific, concentration-dependent uptake of vitellin by the oocytes of Nereis virens (Annelida: Polychaeta) in vitro. J Exp Zool 260:106–115. https://doi.org/10.1002/jez.1402600114
Fischer A, Dorresteijn AWC, Hoeger U (1996) Metabolism of oocyte construction and the origin of histospecificity in the cleaving egg. Lessons from nereid annelids. Int J Develop 40:421–430
Fontaine F, Gevaert MH, Porchet M (1984a) Acylglycerol metabolism in the coelomic constituents during vitellogenesis of Perinereis cultrifera (Annelida Polychaeta). Comp Biochem Physiol B 78:581–584. https://doi.org/10.1016/0305-0491(84)90101-9
Fontaine F, Gevaert MH, Porchet M (1984b) Distribution of neutral lipids in coelomic constituents during oogenesis of Perinereis cultrifera (Annelida Polychaeta). Comp Biochem Physiol A 77:45–50. https://doi.org/10.1016/0300-9629(84)90009-4
Fowler BA, Hildebrand CE, Kojima Y, Webb M (1987) Nomenclature of metallothionein. Experientia Suppl 52:19–22. https://doi.org/10.1007/978-3-0348-6784-9_2
García-Alonso J, Rebscher N (2005) Estradiol signalling in Nereis virens reproduction. Invert Repr Develop 48(1–3):95–100. https://doi.org/10.1080/07924259.2005.9652175
García-Alonso J, Hoeger U, Rebscher N (2006) Regulation of vitellogenesis in Nereis virens (Annelida: Polychaeta): Effect of estradiol-17b on eleocytes. Comp Biochem Physiol A 143(1):55–61. https://doi.org/10.1016/j.cbpa.2005.10.022
Giangrande A, Licciano M, Pagliara P, Gambi MC (2000) Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea. Mar Biol 136(5):847–861. https://doi.org/10.1007/s002279900251
Gruber C, Stürzenbaum SR, Gehring P, Sack R, Hunziker P, Berger B, Dallinger R (2000) Isolation and characterization of a self-sufficient one-domain protein (Cd)-Metallothionein from Eisenia foetida. Eur J Biochem 267:573–582. https://doi.org/10.1046/j.1432-1327.2000.01035.x
Hafer J, Fischer A, Ferenz HJ (1992) Identification of the yolk receptor protein in oocytes of Nereis virens (Annelida, Polychaeta) and comparison with the locust vitellogenin receptor. J Comp Physiol B 162:148–152. https://doi.org/10.1007/BF00398340
Harris JR, Hoeger U, Adrian M (2001) Transmission electron microscopical studies on some haemolymph proteins from the marine polychaete Nereis virens. Micron 32(6):599–613. https://doi.org/10.1016/S0968-4328(00)00051-2
Hauenschild C (1956) Hormonale Hemmung der Geschlechtsreife und Metamorphose bei dem Polychaeten Platynereis dumerilii. Zt Naturforsch B 11:125–132
Hayashi Y, Miclaus T, Engelmann P, Autrup H, Sutherland DS, Scott-Fordsmand JJ (2016) Nanosilver pathophysiology in earthworms: Transcriptional profiling of secretory proteins and the implication for the protein corona. Nanotoxicology 10:303–311. https://doi.org/10.3109/17435390.2015.1054909
Hirigoyenberry F, Lassalle F, Lassegues M (1990) Antibacterial activity of Eisenia fetida andrei coelomic fluid: Transcription and translation of lysozyme and proteins evidenced after bacterial infestation. Comp Biochem Physiol B 95:71–75. https://doi.org/10.1016/0305-0491(90)90250-w
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol Biol Evol 35(2):518–522. https://doi.org/10.1093/molbev/msx281
Hoeger U, Abe H (2004) ß-Alanine and other free amino acids during salinity adaption of the polychaete Nereis japonica. Comp Biochem Physiol A 137(1):161–171. https://doi.org/10.1016/S1095-6433(03)00286-1
Hoeger U, Kunz I (1993) Metabolic enzymes in coelomic cells (eleocytes) of the polychaete Nereis virens: sex specific changes during sexual maturation. Mar Biol 115:653–660. https://doi.org/10.1016/j.cbpb.2010.06.001
Hoeger U, Märker C (1997) Nucleotide pool changes in coelomic cells (eleocytes) of the polychaete Nereis virens during sexual maturation. Exp Biol Online 2–12 (12)
Hoeger U, Märker C, Geier G (1996) Adenylate storage, metabolism and utilization of the polychaete Nereis virens (Annelida, Polychaeta). Experientia 52:481–486
Hoeger U, Rebscher N, Geier G (1999) Metabolite supply in growing oocytes of Nereis virens: role of nucleosides. Hydrobiologia 402:163–174. https://doi.org/10.1023/A:1003792525942
Homa J, Ortmann W, Kolaczkowska E (2016) Conservative mechanisms of extracellular trap formation by annelida Eisenia andrei: serine protease activity requirement. PLoS ONE 11:e0159031. https://doi.org/10.1371/journal.pone.0159031
Hussain MM, Shi J, Dreizen P (2003) Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J Lipid Res 44(1):22–32. https://doi.org/10.1194/jlr.r200014-jlr200
Ishitsuka R, Kobayashi T (2007) Cholesterol and lipid/protein ratio control the oligomerization of a sphingomyelin-specific toxin, lysenin. Biochemistry 46(6):1495–1502. https://doi.org/10.1021/bi061290k
Ito Y, Ayako Y, Hotani T, Fukuda S, Sugimura K, Imoto T (1999) Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur J Biochem 259:456–461. https://doi.org/10.1046/j.1432-1327.1999.00064.x
Jamieson BGM (2006) Reproductive biology and phylogeny of annelida. In: Reproductive biology and phylogeny, vol 4, 1st edn. CRC Press, Boca Raton. https://doi.org/10.1201/9781482280159
Jeong BR, Chung SM, Baek NJ, Koo KB, Baik HS, Joo HS, Chang CS, Choi JW (2006) Characterization, cloning and expression of the ferritin gene from the Korean polychaete, Periserrula leucophryna. J Microbiol 44(1):54–63
Josková R, Šilerová M, Procházková P, Bilej M (2009) Identification and cloning of an invertebrate-type lysozyme from Eisenia andrei. Dev Comp Immunol 33:932–938. https://doi.org/10.1016/j.dci.2009.03.002
Journet AM, Saffaripour S, Wagner DD (1993) Requirement for both D domains of the propolypeptide in von Willebrand factor multimerization and storage. Thromb Haemost 70(6):1053–1057
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285
Kauschke E, Mohrig W (1987) Cytotoxic activity in the coelomic fluid of the annelid Eisenia foetida Sav. J Comp Physiol B 157:77–83. https://doi.org/10.1007/bf00702731
Kauschke E, Pagliara P, Stabili L, Cooper EL (1997) Characterization of proteolytic activity in coelomic fluid of Lumbricus terrestris L (Annelida, Lumbricidae). Comp Biochem Physiol B 116(2):235–242. https://doi.org/10.1016/S0305-0491(96)00248-9
Kauschke E, Mohrig W, Cooper EL (2007) Coelomic fluid proteins as basic components of innate immunity in earthworms. Eur J Soil Biol 43:S110–S115. https://doi.org/10.1016/j.ejsobi.2007.08.043
Kiyokawa E, Makino A, Ishii K, Otsuka N, Yamaji-Hasegawa A, Kobayashi T (2004) Recognition of sphigomyelin by lysenin and lysenin-related protein. Biochemistry 43:9766–9773. https://doi.org/10.1021/bi049561j
Klotz IM, Kurtz DM (1984) Binuclear oxygen carriers: hemerythrin. Accounts Chem Res 17(1):16–22. https://doi.org/10.1021/ar00097a003
Kulakosky PC, Telfer WH (1990) Lipophorin as a yolk precursor in Hyalophora cecropia: Uptake kinetics and competition with vitellogenin. Arch Biochem Biophys 14:269–285. https://doi.org/10.1002/arch.940140406
Lange S, Nussler F, Kauschke E, Lutsch G, Cooper EL, Herrmann A (1997) Interaction of earthworm hemolysin with lipid membranes requires sphingolipids. J Biol Chem 272(33):20884–20892. https://doi.org/10.1074/jbc.272.33.20884
Lange S, Kauschke E, Mohrig W, Cooper EL (1999) Biochemical characteristics of Eiseniapore, a pore-forming protein in the coelomic fluid of earthworms. Eur J Biochem 262(2):547–556. https://doi.org/10.1046/j.1432-1327.1999.00407.x
Lassalle F, Lassegues M, Roch P (1988) Protein analysis of earthworm coelomic fluid - IV. Evidence, activity induction and purification of Eisenia fetida andrei lysozyme (Annelidae). Comp Biochem Physiol B 91:187–192. https://doi.org/10.1016/0305-0491(88)90133-2
Lassegues M, Milochau A, Doignon F, Du Pasquier L, Valembois P (1997) Sequence and expression of an Eisenia fetida-derived cDNA clone that encodes the 40-kDa fetidin antibacterial protein. Eur J Biochem 246:756–762. https://doi.org/10.1111/j.1432-1033.1997.00756.x
Lee YR, Kim YN (1993) Selective transport of coelomic fluid protein into oocytes of a tubicolous polychaete, Pseudopotamilla occelata. Invert Reprod Develop 24(2):119–126. https://doi.org/10.1080/07924259.1993.9672341
Lee BK, Nam HJ, Lee YR (1997) Receptor-mediated transport of vitellin during oogenesis of a polychaete, Pseudopotamilla ocelata. Kor J Biol Sci 1:341–344
Li W, Li S, Zhong J, Zhu Z, Liu J, Wang W (2011) A novel antimicrobial peptide from skin secretions of the earthworm Pheretima guillelmi (Michaelsen). Peptides 32:1146–1150. https://doi.org/10.1016/j.peptides.2011.04.015
Li C, Chen M, Li X, Yang M, Wang Y, Yang X (2017) Purification and function of two analgesic and anti-inflammatory peptides from coelomic fluid of the earthworm, Eisenia foetida. Peptides 89:71–81. https://doi.org/10.1016/j.peptides.2017.01.016
MacMahon BR, Wikens JL, Smith PJS (1997) Invertebrate circulatory systems. In: Dantzler WH (ed) Comparative Physiology. Oxford Univ. Press, New York, pp 931–1008
Maltseva, AL, Kotenko, ON, Kokryakov, VN, Starunov, VV, Krasnodembskaya, AD (2014) Expression pattern of arenicins—the antimicrobial peptides of polychaete Arenicola marina. Front Physiol 5. https://doi.org/10.3389/fphys.2014.00497
Mangum CP, Woodin BR, Bonaventura C, Sullivan B, Bonaventura J (1975) Role of coelomic and vascular hemoglobin in annelid family terebellidae. Comp Biochem Phys A 51(2):281–294. https://doi.org/10.1016/0300-9629(75)90372-2
Marcano L, Nusetti O, Rodriguez-Grau J, Briceño J, Vilas J (1997) Coelomic fluid lysozyme activity induction in the polychaete Eurythoe complanata as a biomarker of heavy metal toxicity. Bull Environ Contam Toxicol 59:22–28. https://doi.org/10.1007/s001289900438
Margoshes M, Vallee BL (1957) A cadmium protein from equine kidney cortex. J Am Chem Soc 79(17):4813–4814. https://doi.org/10.1021/ja01574a064
Marusek CM, Trobaugh NM, Flurkey WH, Inlow JK (2006) Comparative analysis of polyphenol oxidase from plant and fungal species. J Inorg Biochem 100:108–123. https://doi.org/10.1016/j.jinorgbio.2005.10.008
Mazur AI, Klimek M, Morgan AJ, Plytycz B (2011) Riboflavin storage in earthworm chloragocytes and chloragocyte-derived eleocytes and its putative role as chemoattractant for immunocompetent cells. Pedobiologia 54:S37–S42. https://doi.org/10.1016/j.pedobi.2011.09.008
M'Beri M, Debray H, Dhainaut A (1988) Separation of two different populations of granulocytes of Nereis diversicolor (Annelida) by selective agglutination with lectins. Dev Comp Immunol 12(2):279–285. https://doi.org/10.1016/0145-305x(88)90004-3
McKenzie HA, White FH Jr (1991) Lysozyme and α-lactalbumin: structure, function and interrelationships. Adv Prot Chem 41:173–315. https://doi.org/10.1016/s0065-3233(08)60198-9
McLaughlin J (1971) Biochemical studies on Eisenia foetida (Savigny, 1826), the brandling worm - I. Tissue lipids and sterols. Comp Biochem Physiol B 38:147–163. https://doi.org/10.1016/0305-0491(71)90294-X
Milochau A, Lassègues M, Valembois P (1997) Purification, characterization and activities of two hemolytic and antibacterial proteins from coelomic fluid of the annelid Eisenia fetida andrei. Biochim Biophys Acta 1137:123–132. https://doi.org/10.1016/s0167-4838(96)00160-4
Minh B, Nguyen M, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195. https://doi.org/10.1093/molbev/mst024
Nagai T, Kawabata S (2000) A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J Biol Chem 275(38):29264–29267. https://doi.org/10.1074/jbc.M002556200
Nejmeddine A, Dhainautcourtois N, Baert JL, Sautiere P, Fournet B, Boulenguer P (1988) Purification and characterization of a cadmium-binding protein from Nereis diversicolor (Annelida, Polychaeta). Comp Biochem Phys C 89(2):321–326. https://doi.org/10.1016/0742-8413(88)90231-9
Nejmeddine A, Sautiere P, Dhainaut-Courtois N, Baert JL (1992) Isolation and characterization of a Cd-binding protein from Allolobophora caliginosa (Annelida, Oligochaeta): distinction from metallothioneins. Comp Biochem Physiol C 101(3):601–605. https://doi.org/10.1016/0742-8413(92)90093-M
Nejmeddine A, Wouters-Tyrou D, Baert JL, Sautiere P (1997) Primary structure of a myohemerythrin-like cadmium-binding protein, isolated from a terrestrial annelid oligochaete. C R Acad Sci III 320(6):459–468
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300
Nichol H, Law JH, Winzerling JJ (2002) Iron metabolism in insects. Annu Rev Entomol 47:535–559. https://doi.org/10.1146/annurev.ento.47.091201.145237
Ohta N, Shioda S, Sekizawa Y, Nakai Y, Kobayashi H (2000) Sites of expression of mRNA for lysenin, a protein isolated from the coelomic fluid of the earthworm Eisenia foetida. Cell Tissue Res 302(2):263–270. https://doi.org/10.1007/s004410000284
Olivares Fontt E, 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 26:27–34. https://doi.org/10.1016/s0145-305x(01)00048-9
Olsen I, Jantzen E (2001) Sphingolipids in bacteria and fungi. Anaerobe 7:103–112. https://doi.org/10.1006/anae.2001.0376
Opper B, Bognar A, Heidt D, Nemeth P, Engelmann P (2013) Revising lysenin expression of earthworm coelomocytes. Dev Comp Immunol 39(3):214–218. https://doi.org/10.1016/j.dci.2012.11.006
Ovchinnikova, TV, Shenkarev, ZO, Nadezhdin, KD, Balandin, SV, Zhmak, MN, Kudelina, IA, Finkina, EI, Kokryakov, VN, Arseniev, AS (2007) Recombinant expression, synthesis, purification, and solution structure of arenicin. Biochem Biophys Res Com 360(1):156–162. https://doi.org/10.1016/j.bbrc.2007.06.029
Paiva-Silva GO, Cruz-Oliveira C, Nakayasu ES, Maya-Monteiro CM, Dunkov BC, Masuda H, Almeida IC, Oliveira PL (2006) A heme-degradation pathway in a blood-sucking insect. Proc Natl Acad Sci U S A 103(21):8030–8035. https://doi.org/10.1073/pnas.0602224103
Pan, W, Liu, X, Ge, F, Han, J, Zheng, T (2004) Perinerin, a novel antimicrobial peptide purified from the clamworm Perinereis aibuhitensis Grube and its partial characterization. J Biochem 135(3):297–304. https://doi.org/10.1093/jb/mvh036
Pereira LOR, Oliveira PL, Almeida IC, Paiva-Silva GO (2007) Biglutaminyl-biliverdin IX alpha as a heme degradation product in the dengue fever insect-vector Aedes aegypti. Biochemistry 46(23):6822–6829. https://doi.org/10.1021/bi700011d
Périn J-P, Jollès P (1972) The lysozyme from Nephthys hombergi (Annelid). Biochim Biophys Acta 263:683–689. https://doi.org/10.1016/0005-2795(72)90051-7
Plytycz B, Morgan AJ (2011) Riboflavin storage in earthworm chloragocytes/eleocytes in an eco-immunology perspective. Isj-Invert Surviv J 8(2):199–209
Podobnik M, Savory P, Rojko N, Kisovec M, Wood N, Hambley R, Pugh J, Wallace EJ, McNeill L, Bruce M, Liko I, Allison TM, Mehmood S, Yilmaz N, Kobayashi T, Gilbert RJ, Robinson CV, Jayasinghe L, Anderluh G (2016) Crystal structure of an invertebrate cytolysin pore reveals unique properties and mechanism of assembly. Nat Commun 7:11598. https://doi.org/10.1038/ncomms11598
Porchet-Henneré E (1990) Cooperation between different coelomocyte populations during encapsulation response of Nereis diversicolor demonstrated by using monoclonal antibodies. J Invert Pathol 56:353–361. https://doi.org/10.1016/0022-2011(90)90122-M
Porchet-Henneré E, Nejmeddine A, Baert JL, Dhainaut-Courtois N (1987) Selective immunostaining of type-1 granulocytes of the polychaete annelid Nereis diversicolor by a monoclonal-antibody against acadmium-binding protein (Mp-II). Biol Cell 60(3):259–261
Porchet-Hennere E, Vernet G (1992) Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes. Cell Tissue Res 269(1):167–174. https://doi.org/10.1007/bf00384737
Porchet-Hennere E, Dugimont T, Fischer A (1992) Natural killer cells in a lower invertebrate, Nereis diversicolor. Eur J Cell Biol 58(1):99–107
Prochazkova P, Dvorak J, Silerova M, Roubalova R, Skanta F, Halada P, Bilej M (2011) Molecular characterization of the iron binding protein ferritin in Eisenia andrei earthworms. Gene 485(2):73–80. https://doi.org/10.1016/j.gene.2011.06.010
Racovitza E (1895) Sur le role des amibocytes chez les annélides polychètes. C R Acad Sci, Paris 120:464–467
Ratcliffe NA, Rowley AF (1981a) Arthropods to urochordates. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 2. Academic Press, New York
Ratcliffe NA, Rowley AF (1981b) General aspects. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, New York
Roch P, Ville P, Cooper EL (1998) Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coelomic fluid. Dev Comp Immunol 22(1):1–12. https://doi.org/10.1016/s0145-305x(97)00047-5
Roesijadi G, Fowler BA (1991) Purification of invertebrate metallothioneins. Meth Enzymol 205:263–273. https://doi.org/10.1016/0076-6879(91)05106-6
Romieu M (1921) Sur les éléocytes de Perinereis cultrifera (Grube). C R Acad Sci Paris 173:246–249
Ryan RO (1990) Dynamics of insect lipophorin metabolism. J Lipid Res 31:1725–1739
Salzet-Raveillon B, Rentier-Delrue F, Dhainaut A (1993) Detection of mRNA encoding an antibacterial-metalloprotein (MPII) by in situ hybridization with a cDNA probe generated by polymerase chain reaction in the worm Nereis diversicolor. Cell Mol Biol (Noisy-le-grand) 39 (1):105–114
Sánchez-Ferrer Á, Rodríguez-López JN, García-Cánovas F, García-Carmona F (1995) Tyrosinase: a comprehensive review of its mechanism. Biochim Biophys Acta 1247:1–11. https://doi.org/10.1016/0167-4838(94)00204-t
Schenk S, Hoeger U (2009) Lipoprotein mediated lipid uptake in oocytes of polychaetes (Annelida). Cell Tiss Res 337(2):341–348. https://doi.org/10.1007/s00441-009-0817-7
Schenk S, Hoeger U (2010) Lipid accumulation and metabolism in polychaete spermatogenesis: Role of the large discoidal lipoprotein. Mol Reprod Dev 77:710–719. https://doi.org/10.1002/mrd.21208
Schenk S, Hoeger U (2011) Glutathionyl-biliverdin IXa, a new heme catabolite in a marine annelid: sex and cell specific accumulation. Biochimie 93(2):302–316
Schenk S, Harris JR, Hoeger U (2006) A discoidal lipoprotein from the coelomic fluid of the polychaete Nereis virens. Comp Biochem Physiol B 143(2):236–243. https://doi.org/10.1016/j.cbpb.2005.11.012
Schenk S, Krauditsch C, Fruhauf P, Gerner C, Raible F (2016) Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction. Elife 5. https://doi.org/10.7554/eLife.17126
Schikorski D, Cuvillier-Hot V, Leippe M, Boidin-Wichlacz C, Slomianny C, Macagno ER, Salzet M, Tasiemski A (2008) Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. J Immunol 181 (1083–1095). https://doi.org/10.4049/jimmunol.181.2.1083
Schmidt O, Soderhall K, Theopold U, Faye I (2010) Role of adhesion in arthropod immune recognition. Ann Rev Entomol 55:485–504. https://doi.org/10.1146/annurev.ento.54.110807.090618
Schüßler P, Potters E, Winnen R, Bottke W, Kunz W (1995) An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni. Mol Reprod Dev 41(3):325–330. https://doi.org/10.1002/mrd.1080410307
Scott DM (1976) Circadian rhythm of anaerobiosis in a polychaete annelid. Nature 262:811–813. https://doi.org/10.1038/262811a0
Sekizawa Y, Kubo T, Kobayashi H, Nakajima T, Natori S (1997) Molecular cloning of cDNA for lysenin, a novel protein in the earthworm Eisenia foetida that causes contraction of rat vascular smooth muscle. Gene 191(1):97–102. https://doi.org/10.1016/s0378-1119(97)00047-4
Seo J-K, Nam B-H, Go H-J, Jeong M, Lee K-Y, Cho S-M, Lee I-A, Park NG (2016) Hemerythrin-related antimicrobial peptide, msHemerycin, purified from the body of the lugworm, Marphysa sanguinea. Fish Shellfish Immunol 57:49–59. https://doi.org/10.1016/j.fsi.2016.08.018
Shakor AB, Czurylo EA, Sobota A (2003) Lysenin, a unique sphingomyelin-binding protein. FEBS Lett 542(1–3):1–6. https://doi.org/10.1016/s0014-5793(03)00330-2
Silerova M, Prochazkova P, Joskova R, Josens G, Beschin A, De Baetselier P, Bilej M (2006) Comparative study of the CCF-like pattern recognition protein in different Lumbricid species. Dev Comp Immunol 30(9):765–771. https://doi.org/10.1016/j.dci.2005.11.002
Smith VJ, Söderhäll K (1991) A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev Comp Immunol 15:251–261. https://doi.org/10.1016/0145-305x(91)90018-t
Smolenaars MMW, De Morreé A, Kerver J, Van der Horst DJ, Rodenburg KW (2007a) Insect lipoprotein biogenesis depends on an amphipatic ß cluster in apolipophorin II/I and is stimulated by microsomal triglyceride transfer protein. J Lipid Res 48:1955–1965. https://doi.org/10.1194/jlr.M600434-JLR200
Smolenaars MMW, Madsen O, Rodenburg KW, Van der Horst DJ (2007b) Molecular diversity of the large lipid transfer protein superfamily. J Lipid Res 48:489–502. https://doi.org/10.1194/jlr.R600028-JLR200
Soderhall K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10(1):23–28. https://doi.org/10.1016/s0952-7915(98)80026-5
Spaziani E, Havel RJ, Hamilton RL, Hardman DA, Stoudemire JB, Watson RD (1986) Properties of serum high-density lipoproteins in the crab, Cancer antennarius Stimpson. Comp Biochem Physiol B 85(2):307–314. https://doi.org/10.1016/0305-0491(86)90005-2
Stürzenbaum SR, Kille P, Morgan AJ (1998) The identification, cloning and characterization of earthworm metallothionein. FEBS Lett 431(3):437–442. https://doi.org/10.1016/s0014-5793(98)00809-6
Stürzenbaum SR, Winters C, Galay M, Morgan AJ, Kille P (2001) Metal ion trafficking in earthworms. Identification of a cadmium-specific metallothionein. J Biol Chem 276 (36):34013–34018. 10.1074/jbc.M103605200
Sturzenbaum SR, Georgiev O, Morgan AJ, Kille P (2004) Cadmium detoxification in earthworms: from genes to cells. Environ Sci Technol 38(23):6283–6289. https://doi.org/10.1021/es049822c
Swiderska B, Kedracka-Krok S, Panz T, Morgan AJ, Falniowski A, Grzmil P, Plytycz B (2017) Lysenin family proteins in earthworm coelomocytes - Comparative approach. Dev Comp Immunol 67:404–412. https://doi.org/10.1016/j.dci.2016.08.011
Taki H, Baert JL, Dhainaut A (1989) Synthesis and release of vitellogenin-associated phospholipids by the coelomocytes of Perinereis cultifera (Annelida, Polychaeta). Comp Biochem Physiol B 92(1):167–173. https://doi.org/10.1016/0305-0491(89)90330-1
Tasiemski A, Vandenbulcke F, Mitta G, Lemoine J, Lefebvre C, Sautiere PE, Salzet M (2004) Molecular characterization of two novel antibacterial peptides inducible upon bacterial challenge in an annelid, the leech Theromyzon tessulatum. J Biol Chem 279(30):30973–30982. https://doi.org/10.1074/jbc.M312156200
Telfer WH, Pan M-L, Law JH (1991) Lipophorin in developing adults of Hyalophora cecropia: support of yolk formation and preparation for flight. Insect Biochem Mol Biol 21(-):653–663
Tučková L, Rejnek J, Šíma P, Ondřejová R (1986) Lytic activities in coelomic fluid of Eisenia foetida and Lumbricus terrestris. Dev Comp Immunol 10(2):181–189. https://doi.org/10.1016/0145-305X(86)90002-9
Vaillier J, Cadoret MA, Roch P, Valembois P (1985) Protein analysis of earthworm coelomic fluid. III. Isolation and characterization of several bacteriostatic molecules from Eisenia fetida andrei. Dev Comp Immunol 9(1):11–20. https://doi.org/10.1016/0145–305x(85)90055–2
Valembois P, Roch P, Lassegues M, Davant N (1982) Bacteriostatic activity of a chloragogen cell secretion. Pedobiologia 24(4):191–195
Valembois P, Seymour J, Roch P (1991) Evidence and cellular localization of an oxidase activity in the coelomic fluid of the earthworm Eisenia fetida andrei. J Invertebr Pathol 57:177–183
Vetvicka V, Sima P (2009) Origins and functions of annelide immune cells: the concise survey. Isj-Invert Surviv J 6(2):138–143
Wang X, Wang X, Zhang Y, Qu X, Yang S (2003) An antimicrobial peptide of the earthworm Pheretima tschiliensis: cDNA cloning, expression and immunolocalization. Biotechnol Lett 25:1317–1323
Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81(2):569–628. https://doi.org/10.1152/physrev.2001.81.2.569
Weers PM, Van Marrewijk WJ, Beenakkers AM, Van der Horst DJ (1993) Biosynthesis of locust lipophorin. Apolipophorins I and II originate from a common precursor. J Biol Chem 268 (6):4300–4303
Westheide W (2013) Spezielle Zoologie, vol 1. Einzeller und wirbellose Tiere, 3rd edn. Springer-Spektrum, Berlin
Won EJ, Rhee JS, Ra K, Kim KT, Au DW, Shin KH, Lee JS (2011) Molecular cloning and expression of novel metallothionein (MT) gene in the polychaete Perinereis nuntia exposed to metals. Environ Sci Pollut Res Int 19(7):2606–2618. https://doi.org/10.1007/s11356-012-0905-1
Yamaji A, Sekizawa Y, Emoto K, Sakuraba H, Inoue K, Kobayashi H, Umeda M (1998) Lysenin, a novel sphingomyelin-specific binding protein. J Biol Chem 273(9):5300–5306. https://doi.org/10.1074/jbc.273.9.5300
Zhang Y, Cui J, Zhang R, Wang Y, Hong M (2007) A novel fibrinolytic serine protease from the polychaete Nereis (Neanthes) virens (Sars): purification and characterization. Biochimie 89(1):93–103. https://doi.org/10.1016/j.biochi.2006.07.023
Zhang L, Cui W, Chen Q, Ren Q, Zhu Y, Zhang Y (2020) Thymosin-beta12 characteristics and function in Urechis unicinctus. Comp Biochem Physiol B 239:110366. https://doi.org/10.1016/j.cbpb.2019.110366
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Schenk, S., Hoeger, U. (2020). Annelid Coelomic Fluid Proteins. In: Hoeger, U., Harris, J. (eds) Vertebrate and Invertebrate Respiratory Proteins, Lipoproteins and other Body Fluid Proteins. Subcellular Biochemistry, vol 94. Springer, Cham. https://doi.org/10.1007/978-3-030-41769-7_1
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