Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T16:57:53.102Z Has data issue: false hasContentIssue false
  • English
  • Français

Intestinal inflammatory response of powan Coregonus lavaretus (Pisces) to the presence of acanthocephalan infections

Published online by Cambridge University Press:  02 June 2009

B. S. DEZFULI ,
A. LUI ,
G. GIOVINAZZO ,
P. BOLDRINI  and
L. GIARI
B. S. DEZFULI*
Affiliation:
Department of Biology and Evolution, University of Ferrara, St Borsari 46, 44100Ferrara, Italy
A. LUI
Affiliation:
Department of Biology and Evolution, University of Ferrara, St Borsari 46, 44100Ferrara, Italy
G. GIOVINAZZO
Affiliation:
Department of Cellular and Environmental Biology, University of Perugia, St Elce di Sotto06123Perugia, Italy
P. BOLDRINI
Affiliation:
Centre of Electron Microscopy, University of Ferrara, St Borsari 46, 44100Ferrara, Italy
L. GIARI
Affiliation:
Department of Biology and Evolution, University of Ferrara, St Borsari 46, 44100Ferrara, Italy
*
*Corresponding author: Department of Biology and Evolution, University of Ferrara, St Borsari 46, 44100Ferrara, Italy. Tel: +39 0532 455701. Fax: +39 0532 455715. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Immunopathological and ultrastructural studies were carried out on the gut of 30 specimens of powan Coregonus lavaretus (L.) from Lake Piediluco, Italy. The digestive tracts of 10 (33·3%) of the powan were found to harbour an acanthocephalan Dentitruncus truttae (Sinzar 1955). The numerous trunk spines of D. truttae reduced the number of mucosal folds near the parasite site of infection. The acanthocephalan induced hyperplasia and hypertrophy of the intestinal mucous cells and many worms were surrounded with an adherent mucous gel. Near the site of acanthocephalan attachment, the number of mucous cells was significantly higher (P<0·01) in comparison to those found in uninfected intestines. Rodlet cells (RCs) were present in the epithelial layer in both infected and uninfected fish, with no significant difference in the numbers observed (P>0·05). In infected intestine, mast cells were more abundant than in uninfected gut (P<0·01). Migration of the mast cells and their intense degranulation at the site of infection were suggested. Immunohistochemical tests applied to sections of intestinal tissue of both infected and uninfected powan revealed that the parasitized C. lavaretus had a larger number of mast cells positive for met-enkephalin and serotonin antisera.

Keywords

histopathologyimmune cellsCoregonus lavaretusparasitized fishDentitruncus truttaeAcanthocephala
Type
Research Article
Information
Parasitology , Volume 136 , Issue 8 , July 2009 , pp. 929 - 937
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bosi, G., Arrighi, S., Di Giancamillo, A. and Domeneghini, G. (2005 a). Histochemistry of glycoconjugates in mucous cells of Salmo trutta uninfected and naturally parasitized with intestinal helminths. Diseases of Aquatic Organisms 64, 45–51. doi: 10.3354/dao064045.CrossRefGoogle ScholarPubMed
Bosi, G., Domeneghini, C., Arrighi, S., Giari, L., Simoni, E. and Dezfuli, B. S. (2005 b). Response of neuroendocrine system of the intestine of Leuciscus cephalus (L., 1758) naturally infected with Pomphorhynchus laevis Müller, 1776 (Acanthocephala). Histology and Histopathology 20, 509–518.Google Scholar
Castro, G. A. (1992). Intestinal physiology in the parasitized host: integration, disintegration, and reconstruction of systems. Annals of the New York Academy of Sciences 664, 369–379. doi: 10.1111/j.1749-6632.1992.tb39775.x.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Arrighi, S., Domeneghini, C. and Bosi, G. (2000 a). Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta Linnaeus naturally infected with Cyathocephalus truncatus Pallas (Cestoda). Journal of Fish Diseases 23, 265–273. doi: 10.1046/j.1365-2761.2000.00234.x.CrossRefGoogle Scholar
Dezfuli, B. S. and Giari, L. (2008). Mast cells in the gills and intestines of naturally infected fish: evidence of migration and degranulation. Journal of Fish Diseases 31, 845–852. doi:10.1111/j.1365-2761.2008.00961.x.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Pironi, F., Giari, L., Domeneghini, C. and Bosi, G. (2002). Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta. Diseases of Aquatic Organisms 51, 27–35. doi: 10.3354/dao051027.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Pironi, F., Simoni, E., Shinn, A. P. and Giari, L. (2007). Selected pathological, immunohistochemical and ultrastructural changes associated with an infection by Diphyllobothrium dendriticum (Nitzsch, 1824) (Cestoda) plerocercoids in Coregonus lavaretus (L.) (Coregonidae). Journal of Fish Diseases 30, 471–482. doi: 10.1111/j.1365-2761.2007.00833.x.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Simoni, E., Rossi, R. and Manera, M. (2000 b). Rodlet cells and other inflammatory cells of Phoxinus phoxinus infected with Raphidascaris acus (Nematoda). Diseases of Aquatic Organisms 43, 61–69. doi: 10.3354/dao043061.CrossRefGoogle ScholarPubMed
Fairweather, I. (1997). Peptides: an emerging force in host response to parasitism. In Parasites and Pathogens: Effects on Host Hormones and Behaviour (ed. Beckage, N. E.), pp. 113–139. Chapman and Hall, New York, USA.CrossRefGoogle Scholar
Flaño, E., Lopez-Fierro, P., Razquin, B. E. and Villana, A. (1996). In vitro differentiation of eosinophilic granular cells in Renibacterium salmoninarum-infected gill cultures from rainbow trout. Fish and Shellfish Immunology 6, 173–184.CrossRefGoogle Scholar
Hamers, R. L., Jens Stürenberg, F. J. and Taraschewski, H. (1992). In vitro study of the migratory and adherent responses of fish leucocytes to the eel-pathogenic acanthocephalan Paratenuisentis ambiguus (Van Cleave, 1921) Bullock et Samuel, 1975 (Eoacanthocephala: Tenuisentidae). Fish and Shellfish Immunology 2, 43–51.CrossRefGoogle Scholar
Hoste, H. (2001). Adaptive physiological process in the host during gastrointestinal parasitism. International Journal for Parasitology 31, 231–244. doi:10.1016/S0020-7519(00)00167-3.CrossRefGoogle ScholarPubMed
Jordanova, M., Miteva, N. and Rocha, E. (2007). A quantitative study of the eosinophilic granule cells and rodlet cells during the breeding cycle of Ohrid trout, Salmo letnica Kar. (Teleostei, Salmonidae). Fish and Shellfish Immunology 23, 473–478. doi:10.1016/j.fsi.2006.11.004.CrossRefGoogle Scholar
Kent, M. L., Powell, M. D., Kieser, D., Hoskins, G. E., Speare, D. J. and Burka, J. F. (1993). Unusual eosinophilic granule cell proliferation in coho salmon (Oncorhynchus kisutch). Journal of Comparative Pathology 109, 129–140. doi:10.1016/S0021-9975(08)80257-5.CrossRefGoogle ScholarPubMed
Khan, N. A. and Deschaux, P. (1997). Role of serotonin in fish immunomodulation. Journal of Experimental Biology 200, 1833–1838.CrossRefGoogle ScholarPubMed
Lamont, J. T. (1992). Mucus: the front line of intestinal mucosal defense. Annals of the New York Academy of Sciences 664, 190–201. doi: 10.1111/j.1749-6632.1992.tb39760.x.CrossRefGoogle ScholarPubMed
Leino, R. L. (1996). Reaction of rodlet cells to a myxosporean infection in kidney of the bluegill, Lepomis macrochirus. Canadian Journal of Zoology 74, 217–225. doi:10.1139/z96-027.CrossRefGoogle Scholar
Manera, M. and Dezfuli, B. S. (2004). Rodlet cells in teleosts: a new insight into their nature and functions. Journal of Fish Biology 65, 597–619. doi:10.1111/j.0022-1112.2004.00511.x.CrossRefGoogle Scholar
Manera, M., Simoni, E. and Dezfuli, B. S. (2001). Effect of dexamethasone administration on occurrence and ultrastructure of rodlet cells in Carassius auratus L. with particular reference to bulbus arteriosus. Journal of Fish Biology 59, 1239–1248. doi: 10.1111/j.1095-8649.2001.tb00188.x.CrossRefGoogle Scholar
Manjili, M. H., France, M. P., Sangster, N. C. and Rothwell, T. L. W. (1998). Quantitative and qualitative changes in intestinal goblet cells during primary infection of Trichostrongylus colubriformis high and low responder guinea pigs. International Journal for Parasitology 28, 761–765. doi:10.1016/S0020-7519(98)00026-5.CrossRefGoogle ScholarPubMed
Mekori, Y. A. (2004). The mastocyte: the “other” inflammatory cell in immunopathogenesis. Journal of Allergy and Clinical Immunology 114, 52–57. doi:10.1016/j.jaci.2004.04.015.CrossRefGoogle ScholarPubMed
Miller, H. R. P. and Huntley, J. F. (1982). Protection against nematodes by intestinal mucus. Advances in Experimental Medicine and Biology 144, 243–245.CrossRefGoogle ScholarPubMed
Mulero, I., Sepulcre, M. P., Meseguer, J., Garcia-Ayala, A. and Mulero, V. (2007). Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response. Proceedings of the National Academy of Sciences, USA 104, 19434–19439. doi:10.1073/pnas.0704535104.CrossRefGoogle ScholarPubMed
Murray, H. M., Leggiadro, C. T. and Douglas, S. E. (2007). Immunocytochemical localization of pleurocidin to the cytoplasmic granules of eosinophilic granular cells from the winter flounder gill. Journal of Fish Biology 70, 336–345. doi: 10.1111/j.1095-8649.2007.01452.x.CrossRefGoogle Scholar
O'Dorisio, M. S. and Panerai, A. (1990). Neuropeptides and immunopeptides: messengers in a neuroimmune axis. Annals of the New York Academy of Sciences 594, 1–503. doi: 10.1111/j.1749-6632.1990.tb40462.x.Google Scholar
Radulovic, J., Mancev, Z., Stanojevic, S., Vsiljevic, T., Kovacevic-Jovanovic, V. and Pesic, G. (1996). Modulation of humoral immune response by central administration of leucine-enkephalin: effects of mu, delta and kappa opioid receptor antagonists. Journal of Neuroimmunology 65, 155–161. doi:10.1016/0165-5728(96)00017-3.CrossRefGoogle ScholarPubMed
Reichlin, S. (1999). Neuroendocrinology of infection and the innate immune system. Recent Progress in Hormone Research 54, 133–183.Google ScholarPubMed
Reite, O. B. (1997). Mast cells/eosinophilic granule cells of salmonids: staining properties and responses to noxious agents. Fish and Shellfish Immunology 7, 567–584.CrossRefGoogle Scholar
Reite, O. B. (1998). Mast cells/granule cells of teleostean fish: a review focusing on staining properties and functional responses. Fish and Shellfish Immunology 8, 489–513.CrossRefGoogle Scholar
Reite, O. B. (2005). The rodlet cells of teleostean fish: their potential role in host defence in relation to the role of mast cells/eosinophilic granule cells. Fish and Shellfish Immunology 19, 253–267. doi:10.1016/j.fsi.2005.01.002.CrossRefGoogle Scholar
Reite, O. B. and Evensen, Ø. (2006). Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish and Shellfish Immunology 20, 192–208. doi:10.1016/j.fsi.2005.01.012.CrossRefGoogle Scholar
Rocha, J. S. and Chiarini-Garcia, H. (2007). Mast cell heterogeneity between two different species of Hoplias sp. (Characiformes: Erythrinidae): response to fixatives, anatomical distribution, histochemical contents and ultrastructural features. Fish and Shellfish Immunology 22, 218–229. doi:10.1016/j.fsi.2006.05.002.CrossRefGoogle ScholarPubMed
Sharkey, K. A. (1992). Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Annals of the New York Academy of Sciences 664, 425–442. doi: 10.1111/j.1749-6632.1992.tb39781.x.CrossRefGoogle ScholarPubMed
Silphaduang, U. and Noga, E. (2001). Peptide antibiotics in mast cells of fish. Nature, London 414, 268–269. doi:10.1038/35104690.CrossRefGoogle ScholarPubMed
Silphaduang, U., Colorni, A. and Noga, E. J. (2006). Evidence for widespread distribution of piscidin antimicrobial peptides in teleost fish. Diseases of Aquatic Organisms 72, 241–252. doi: 10.3354/dao072241.CrossRefGoogle ScholarPubMed
Taraschewski, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179. doi:10.1016/S0065-308X(00)46008-2.CrossRefGoogle ScholarPubMed
Temkin, R. J. and McMillan, D. B. (1986). Gut-associated lymphoid tissue (GALT) of the goldfish, Carassius auratus. Journal of Morphology 190, 9–26. doi: 10.1002/jmor.1051900103.CrossRefGoogle ScholarPubMed
Vallejo, A. N. and Ellis, A. E. (1989). Ultrastructural study of the response of eosinophilic granule cells to Aeromonas salmonicida extracellular products and histamine liberators in rainbow trout, Salmo gairdneri Richardson. Developmental and Comparative Immunology 13, 133–148. doi:10.1016/0145-305X(89)90028-1.CrossRefGoogle ScholarPubMed
Vigliano, R., Bermúdez, J. M., Nieto, M. I. and Quiroga, F. A. (2008). Development of rodlet cells in the gut of turbot (Psetta maxima L.): relationship between their morphology and S100 protein immunoreactivity. Fish and Shellfish Immunology. doi: 10.1016/j.fsi.2008.02.016.Google ScholarPubMed