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Department of Evolutionary Immunology, Institute Of CORE Metadata, citation and similar papers at core.ac.uk Provided by Jagiellonian Univeristy Repository ACTA BIOLOGICA CRACOVIENSIA Series Zoologia 54: 11–17, 2012 RESTO R ATION OF COELOMO C YTES IN THE EA R THWO R M DEN D ROBAENA VENETA Ma ł g o r z a t a Kl i M e K *, Je r z y Kr u K ** a n d Ba r B a r a Pł y t y c z *1 * Department of Evolutionary Immunology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Cracow, Poland ** Faculty of Biochemistry, Biophysics, and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Cracow, Poland Accepted September 28, 2012 We have previously shown that Dendrobaena veneta belongs to the earthworm species which possesses two main cohorts of coelomocytes, namely amoebocytes and autofluorescent eleocytes, the latter storing moderate amounts of riboflavin. The aim of the present experiments performed at 17oC was to follow the restoration of amoebocytes and eleocytes, as well as riboflavin stores in eleocytes after experimental extrusion of coelomocyte-containing coelomic fluid through the dorsal pores induced by electrostimulation (4.5V, 1 min). The analyses were conducted using a combination of cell counts, flow cytometric detection of eleocytes, and spectrofluorimetric measurements of ribofla- vin in coelomocyte lysates. It has been found that the depleted coelomocyte system recovers slowly. The number of amoebocytes reaches the level characteristic of that in undisturbed worms in 4 weeks, while the number of elecytes is still below the control level 6 weeks after extrusion. The amount of riboflavin stored in recovering chloragocyte- derived eleocytes is higher than that in mature eleocytes for at least 4 weeks. Key words: Earthworms, coelomocytes, amoebocytes, eleocytes, riboflavin InTroducTIon wide range of organic wastes are often exposed to high diversity of microorganisms; thus, their im- In natural and semi-natural conditions Dendro- mune system is strongly challenged by microbial baena veneta inhabits dung and compost heaps. antigens and various sorts of pollutants and has It is also cultured on municipal sludge (lo e h r et to be very efficient to cope with them successfully. al., 1985; lo f t s -ho l M i n , 1986) or paper sludge Therefore it is worthwhile to explore the mecha- (fa y o l l e et al., 1997) for the fishing bait market nisms of immunity of earthworm species adapted and/or vermicomposting (for a review see Mo r g a n , to such extreme antigenic challenges. 2010; ya d a v and ga r g , 2011). composting spe- Earthworm immunity comprises cellular and cies, like D. veneta and Eisenia sp., consuming a humoral defense mechanisms, recently reviewed 1 e-mail: [email protected] PL ISSN 0001-530X © Polish Academy of Sciences, Cracow 2012 12 Klimek et al. by Bi l e J et al. (2011). Like other annelid inverte- MaTErIaLs and METhods brates, earthworms possess the metameric coe- lomic cavity filled with coelomic fluid containing Earthworms various antimicrobial factors like lysozyme and antimicrobial peptides and free wandering cells Adult Dendrobaena veneta (oligochaeta; Lumbri- named coelomocytes. The earthworm coelomo- cidae), purchased from the commercial supplier cytes consist of amoebocytes, being classical im- (EKARGo, słupsk), were reared in commercial soil munocytes (according to ot t a v i a n i ’s nomenclature, (PPuh BIoVITa, Tenczynek) under controlled la- 2011), plus a species-specific portion of eleocytes, boratory conditions (17oc; 12:12 Ld). The worms being detached chloragocytes derived from the were kept in plastic boxes with perforated lids chloragogen tissue that surrounds the intestine. and the moisture level was checked weekly. The The chloragocytes/eleocytes, but not amoebo- worms were fed ad libitum a mixed diet comprised cytes, exhibit autofluorescence, which predispo- of dried/boiled nettle (Urtica dioica) and dandelion ses them to flow cytometric analysis (ch o l e w a et (Taraxacum officinale) leaves, boiled/dried tea lea- al., 2006). This autofluorescence is restricted to ves, and powdered commercial mouse pellets. The chloragosomal vesticles (Pl y t y c z et al., 2007) and experiments were performed in May-June. comes from – among other sources – riboflavin (Ko z i o l et al., 2006; cy g a l et al., 2007). riboflavin (vitamin B2) plays an important role in immunity restoration of the coelomocyte system of animals (e.g. Po w e r s , 2003; ve r d r e n g h and ta r - K o w s K i , 2005) and plants (do n g and Be e r , 2000; at the start of the six-week experiments, 30 in- as a i et al., 2010), and it is responsible for quorum dividuals with similar body weight (1.27+0.23 g) sensing in bacteria (ra J a M a n i et al., 2008; at K i n s o n were put into 5 separate boxes with fresh soil co- and wi l l i a M s , 2009). The amount of riboflavin sto- vered with perforated lids, forming 5 experimen- red in eleocytes is species-specific (Pl y t y c z et al. tal groups, 6 worms per group. The worms were 2006) and changes in a species-specific manner in subjected to electrostimulation for coelomocyte response to various edaphic factors (Pl y t y c z et al., extrusion, at various intervals of time before the 2011; Pl y t y c z & Mo r g a n , 2011). end of the experiments. Thus, they had various coelomocyte-containing coelomic fluid can be time periods for recovery of their coelomocyte sy- expelled through dorsal pores during convulsive stems: 6 weeks (6W), 4 weeks (4W), 2 weeks (2W), body movements of worms stressed by various and 1 day (1d). after 6 weeks from the start of the mechanical stimuli (e.g. predators) or chemical experiments all these animals, their body weight factors. The presence of dorsal pores is commonly reaching 1.66+0.33 g, were once again subjected exploited for the non-invasive quantitative retri- to electrostimulation to assess the recovery of the eval of coelomocyte-containing coelomic fluid of coelomocyte system, while the intact animals from worms stimulated by alcohol (co o P e r et al., 1995), the last box were electrostimulated for the first ultrasounds (he n d a w i et al., 2004) or mild electric time and served as the control group with no time current (ro c h et al., 1979), the latter procedure to recover (0d) (Fig. 1). being applied also in the present studies. Dendroabena veneta belongs to the species with a high number of eleocytes storing moderate coelomocyte extrusion amounts of riboflavin which is also accumulated in chloragocytes of the chloragogen tissue (Ma z u r The earthworms were stimulated for 1 minute with et al., 2011; Pl y t y c z and Mo r g a n 2011). We have an electrical current (4.5V) to expel coelomic flu- previously shown that restoration of the coelomo- id with suspended coelomocytes through the dor- cyte number of D. veneta after experimental ex- sal pores. Briefly, the weighed earthworms were trusion is a long-lasting temperature-dependent individually placed in Petri dishes containing 3 process (ol c h a w a et al. 2003). The aim of the pre- mL of extrusion fluid (phosphate-buffered saline, sent research is to continue these investigations PBs, supplemented with 2.5 g/L ethylenediami- focusing on restoration of riboflavin-storing eleo- ne tetra-acetic acid, EdTa; sigma-aldrich); 2mL cytes. samples of the extruded coelomocyte suspensions Restoration of Earthworm Coelomocytes 13 6W by producing dot plots of cell size versus FL1 au- (1) G N I T tofluorescence. S E T 4W (2) R O F spectrofluorimetry and analysis L S A T 2W V N E E (3) I R M I T spectrofluorometric measurements were perfor- R E E 1D R P med on 2 mL coelomocyte-suspension lysates (ly- X E E (4) T sed with 2% Triton; sigma-aldrich) using a Per- Y F C O O kin-Elmer Ls50B spectrofluorimeter. Emission M T O R L A (5) spectra of riboflavin were recorded in the 380-680 E T S O 0D C nm range (lambda at 370 nm), while excitation spectra were recorded in the 300-500 nm range (lambda at 525 nm). The spectrofluorimetric si- -6w -4w -2w -1d 0 gnatures of unbound riboflavin were characteri- TIME BEFORE TESTING sed by two maxima (at 370 nm and 450 nm) in the excitation spectrum, and a maximum at 525 nm Fig. 1. scheme for experiments on restoration of coelomo- in the emission spectrum. arbitrary units (au) of cytes of Dendrobaena veneta depleted by extrusion induced fluorescence were recorded using Microsoft Excel Fig. 1 by electrostimulation. at the start of the experiments 30 worms with similar body weight were divided into 5 experi- v. 97. The amount of riboflavin in the sample was mental groups (6 worms per group) and put into fresh soil proportional to the maximum at 525 nm in the samples. The worms from groups 1-4 were stimulated for co- emission spectrum. elomocyte extrusion at selected time points (grey marks), i.e. 6 weeks (-6w), 4 weeks (-4w), 2 weeks (-2w) or 1 day (-1d) before the end of the experiments at time 0, while group 5 Statistical analysis served as the control. at the end of the experiments (time 0) coelomocytes from all the five groups of worms were extruded by electrostimulation (black marks) and comparisons were coelomocyte-connected parameters were calcula- made between the control worms stimulated for the first time ted using Microsoft Excel version 97.
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