RESEARCH PAPER
Phenoloxidase is involved in the immune reaction of Helix lucorum to parasitic infestation by dicrocoeliid trematode
			
	
 
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				1
				Veterinary  Division,  Vocational  School  of  Gevas,  Van  Yuzuncu  Yil  University,  Van,  Turkey
				 
			 
						
				2
				Department  of  Parasitology,  Faculty  of  Medicine,  Van  Yuzuncu  Yil  University,  Van,  Turkey
				 
			 
										
				
				
		
		 
			
			
		
		
		
		
		
		
	
							
					    		
    			 
    			
    				    					Corresponding author
    					    				    				
    					Ahmet Hakan  Unlu   
    					Veterinary Division, Vocational School of Gevas, Yuzuncu Yil University, Van, Turkey
    				
 
    			
				 
    			 
    		 		
			
												 
		
	 
		
 
 
Ann Agric Environ Med. 2021;28(3):426-429
		
 
 
KEYWORDS
TOPICS
ABSTRACT
Introduction:
Phenoloxidases  are  known  to  play  a  role  in  the  immune  defences  of  arthropods  and  molluscs.  In  the  invertebrates, phenoloxidases mediate three major physiologically important processes: sclerotization, wound healing, and defence reactions. Helix lucorum serve as the first intermediate host for the larval stages of dicrocoeliid trematodes which infects animals as well as human beings.
Objective:
The  aim  of  the  study  is  to  investigate  the  effect  of  larval  forms  of  dicrocoeliid  trematodes  to  phenoloxidase  acitivity in H. lucorum, Linneaus, 1758, in Bitlis, Turkey. The effect of the snail’s shell colour to phenoloxidase activity was also investigated.
Material and methods:
Land snails (n=200) were collected by hand from their natural habitats during the period May – June 2019 in Bitlis, Turkey. Evaluation of the process was performed by measuring immune reaction of the snails against larval forms of dicrocoeliid trematodes. Phenoloxidase activity assay was carried out using a spectrophotometer device based on 3,4-Dihydroxy-L-phenylalanine (L-dopa) hydrolysis.
Results:
The natural infection rate of the land snails with the developmental stages of dicrocoeliid trematodes was 20%. Phenoloxidase activity was found to be significantly higher (*p<0.05) in larval forms of dicrocoeliid trematodes infected snails when compared with non-infected snails. No effect of shell colours to phenoloxidase activity was observed.
Conclusions:
To the best of the authors’ knowledge, this study is the first to report that the phenoloxidase system is involved in the immune reaction of Helix lucorum to parasitic infestation by larval forms of dicrocoeliid trematodes.
		
	
		
Ahmet  Hakan  Unlu,  Abdurrahman  Ekici.  Phenoloxidase  is  involved  in  the  immune  reaction  of  Helix  lucorum  to  parasitic  infestation  by  dicrocoeliid  trematode.  Ann  Agric  Environ  Med. Doi: 10.26444/aaem/140319
REFERENCES (34)
			
			
			
	3.
	
		Stączek S, Grygorczuk K, Zdybicka-Barabas A, et al. Different faces of phenoloxidase in animals. Postepy Biochemi. 2017; 63(4): 315–325.
		
	 
	 
 			
			
	5.
	
		Le Clec’h W, Anderson TJ, Chevalier FD. Characterization of haemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection. Parasites Vectors. 2016; 9(1): 1–11. 
https://doi.org/10.1186/s13071....
 
		
	 
	 
 			
	6.
	
		Leicht K, Jokela J, Seppälä O. An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecol Evol. 2013; 3(15): 4861–4871. 
https://doi.org/10.1002/ece3.8....
 
		
	 
	 
 			
	7.
	
		Quinn EA, Malkin SH, Rowley AF, et al. Laccase and catecholoxidase activities contribute to innate immunity in slipper limpets, Crepidula fornicata. Dev Comp Immunol. 2020; 110: 103724. 
https://doi.org/10.1016/j.dci.....
 
		
	 
	 
 			
	8.
	
		De Melo ES, Brayner FA, Junior NCP, et al. Investigation of defense response and immune priming in Biomphalaria glabrata and Biomphalaria straminea, two species with different susceptibility to Schistosoma mansoni. Parasitol Res. 2020; 119(1): 189–201. 
https://doi.org/10.1007/s00436....
 
		
	 
	 
 			
			
	10.
	
		Noothuan N, Amparyup P, Tassanakajon A. Melanization inhibition protein of Penaeus monodon acts as a negative regulator of the prophenoloxidase-activating system. Dev Comp Immunol. 2017; 72: 97–102. 
https://doi.org/10.1016/j.dci.....
 
		
	 
	 
 			
	11.
	
		Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008; 29(6): 263–271. 
https://doi.org/10.1016/j.it.2....
 
		
	 
	 
 			
			
	13.
	
		Olsen OW. Animal parasites: their life cycles and ecology. New York: Dover Publishing; 1986.
		
	 
	 
 			
	14.
	
		Otranto D, Traversa D. A review of dicrocoeliosis of ruminants including recent advances in the diagnosis and treatment. Vet Parasitol. 2002; 107(4): 317–335. 
https://doi.org/10.1016/s0304-....
 
		
	 
	 
 			
	15.
	
		Conte R. Heliciculture: purpose and economic perspectives in the European community. IST Journal, 2015.
		
	 
	 
 			
	16.
	
		Gliński Z, Jarosz J. Molluscan immune defenses. Arch Immunol Ther Exp. 1997; 45(2–3): 149–155.
		
	 
	 
 			
	17.
	
		Schütt H. Turkish Land Snails, 1758–2000. Vollständig Revidierte und Erweiterte Auflage, Natur & Wissenschaft, 2005.
		
	 
	 
 			
	18.
	
		Renwrantz L, Schäncke W, Harm H, et al. Discriminative ability and function of the immunobiological recognition system of the snail Helix pomatia. J Comp Physiol. 1981; 141(4): 477–488.
		
	 
	 
 			
	19.
	
		Segun AO. Land snails (Dissection guides of common tropical animals). Ethiope Publications, 1973.
		
	 
	 
 			
	20.
	
		Seppälä O, Jokela J. Maintenance of genetic variation in immune defense of a freshwater snail: role of environmental heterogeneity. Evolution. 2010; 64(8): 2397–2407. 
https://doi.org/10.1111/j.1558....
 
		
	 
	 
 			
	21.
	
		Rajendran S, Vasudevan S. Activation of prophenoloxidase and hyperglycemia as indicators of microbial stress in the blue swimmer crab Portunus pelagicus. Mar Pollut Bull. 2020; 160: 111711. 
https://doi.org/10.1016/j.marp....
 
		
	 
	 
 			
			
	23.
	
		Yildirim MZ, Kebapci U, Gumus BA. Edible snails (Terrestrial) of Turkey. Turk J Zool. 2004; 28(4): 329–335.
		
	 
	 
 			
	24.
	
		Eser  M,  Kartal  K,  Navruz  FZ.  The  Prevalence  Of  Dicrocoeliidae  (Digenea) Larval Stages In The First Intermediate Host Helix Lucorum, 
1758 In Eskisehir And Bartin Provinces Of Turkey. Eskisehir Tech Univ J Sci Tech. 2021; 10(1): 38–43. 
https://doi.org/10.18036/estub... 
		
	 
	 
 			
	25.
	
		Kartal K, Mustafa K, Mustafa E. The Prevalance of larval stages of small liver fluke Dicrocoelium dendriticum in the first intermediate host Helix lucorum Linnaeus, 1758 (Mollusca: Pulmonata) in Afyonkarahisar district. Kocatepe Vet J. 2015; 8(1): 51–55. 
https://doi.org/10.18036/estub....
 
		
	 
	 
 			
	26.
	
		Unlu AH, Bilgic HB, Eren H, Karagenc T. Prevalence of Larval-Stage Dicrocoeliidae (Digenea) Trematodes in Helix lucorum (Mollusca: Pulmonata) in Van Province. Turk J Parasitology. 2017; 41(4): 204–207. 
https://doi.org/10.5152/tpd.20....
 
		
	 
	 
 			
	27.
	
		Gerdol M, Gomez-Chiarri M, Castillo MG, et al. Immunity in molluscs: recognition and effector mechanisms, with a focus on bivalvia. In Advances in Comparative Immunology. Cham: Springer; 2018. p. 225–341. 
https://doi.org/10.1007/978-3-....
 
		
	 
	 
 			
	28.
	
		Zhou S, Zhao L, Zhao T. Phenol oxidase activity of Oncomelania snails in different ages and seasons. Chin J Zoonoses. 2010; 26(9): 856–861.
		
	 
	 
 			
	29.
	
		Amparyup P, Charoensapsri W, Tassanakajon A. Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish Shellfish Immunol. 2013; 34(4): 990–1001. 
https://doi.org/10.1016/j.fsi.....
 
		
	 
	 
 			
	30.
	
		Quinn EA, Malkin SH, Rowley AF, et al. Laccase and catecholoxidase activities contribute to innate immunity in slipper limpets, Crepidula fornicata. Dev Comp Immunol. 2020; 110: 103725. 
https://doi.org/10.1016/j.dci.....
 
		
	 
	 
 			
	31.
	
		Ito S, Konuma J. Disruptive selection of shell colour in land snails: a mark–recapture study of Euhadra peliomphala simodae. Biol J Linn Soc. 2020; 129(2): 323–333. 
https://doi.org/10.1093/biolin....
 
		
	 
	 
 			
			
	33.
	
		Scheil AE, Hilsmann S, Triebskorn R, et al. Shell colour polymorphism, injuries and immune defense in three helicid snail species, Cepaea hortensis, Theba pisana and Cornu aspersum maximum. Results Immunol. 2013; 3: 73–78. 
https://doi.org/10.1016/j.rini....
 
		
	 
	 
 			
	34.
	
		Scheil AE, Hilsmann S, Triebskorn R, et al. Shell colouration and parasite tolerance in two helicoid snail species. J Invertebr Pathol. 2014; 117: 1–8. 
https://doi.org/ 10.1016/j.jip.2014.01.003.