In vitro immunotoxicity of environmentally representative antibiotics to the freshwater mussel Elliptio complanata

Environmental Pollution

Volumn 169, Issue , 2012, Pages 50-58

  Gust, M ^a,b   Gelinas M ^a   Fortier, M ^c   Fournier, M ^c   Gagne F ^a,c  

^a ENVIRONMENT CANADA   (Canada)

^b CEMAGREF   (France)

^c INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Antibiotics; Hemocytes; Immunotoxicity; Municipal effluents; Mussels

Indexed keywords

CIPROFLOXACIN; CUMULATIVE EFFECTS; FINE PARTICLES; FRESHWATER MUSSELS; HEMOCYTES; IMMUNE RESPONSE; IMMUNOTOXICITY; IN-VITRO; MAJOR CITIES; MUNICIPAL EFFLUENTS; MUSSELS; NOVOBIOCIN; OXYTETRACYCLINES (OTC); SULFAMETHOXAZOLE; TOXIC EFFECT; TRIMETHOPRIM; URBAN WASTEWATER; WASTEWATER EFFLUENTS;

ANTIBIOTICS; MICROORGANISMS; SHELLFISH; WASTEWATER TREATMENT;

EFFLUENTS;

CIPROFLOXACIN; ERYTHROMYCIN; LYSOZYME; NITRIC OXIDE; NOVOBIOCIN; OXYTETRACYCLINE; SULFAMETHOXAZOLE; TRIMETHOPRIM; ANTIINFECTIVE AGENT; FRESH WATER;

ANTIBIOTICS; BIOACCUMULATION; EFFLUENT; ENVIRONMENTAL ASSESSMENT; IMMUNE RESPONSE; IMMUNOASSAY; MICROORGANISM; MOLLUSC; TOXICITY; WASTEWATER;

ARTICLE; CONTROLLED STUDY; EFFLUENT; ELLIPTIO COMPLANATA; ENZYME ACTIVITY; FILTRATION; IMMUNE RESPONSE; IMMUNOTOXICITY; IN VITRO STUDY; LYMPHOCYTE; MICROORGANISM; MUSSEL; NONHUMAN; PHAGOCYTOSIS; URBAN AREA; WASTE WATER MANAGEMENT; WATER POLLUTION; ANIMAL; BIVALVE; BLOOD CELL; DRUG EFFECT; ENVIRONMENTAL EXPOSURE; IMMUNITY; IMMUNOLOGY; SEWAGE; WATER POLLUTANT;

ELLIPTIO COMPLANATA;

ANIMALS; ANTI-BACTERIAL AGENTS; BIVALVIA; ENVIRONMENTAL EXPOSURE; FRESH WATER; HEMOCYTES; IMMUNITY; SEWAGE; WATER POLLUTANTS, CHEMICAL;

EID: 84861884631     PISSN: 02697491     EISSN: 18736424     Source Type: Journal    
DOI: 10.1016/j.envpol.2012.05.020     Document Type: Article

References (56)

1. Akaishi, F.M., St-Jean, S.D., Bishay, F., Clarke, J., Rabitto, I.d.S., Ribeiro, C.A.D.O., 2007. Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquatic Toxicology 82, 1-14. (Pubitemid 46442875)
2. Besse, Jean-Philippe, Christine, Kausch-Barreto, Garric, Jeanne, 2008. Exposure assessment of pharmaceuticals and their metabolites in the aquatic environment: application to the French situation and preliminary prioritization. Human and Ecological Risk Assessment: An International Journal 14 (4), 665-695.
3. Beschin, A., Bilej, M., Torreele, E., De Baetselier, P., 2001. On the existence of cytokines in invertebrates. Cellular and Molecular Life Sciences 58, 801-814. (Pubitemid 32553035)
4. Betti, M., Ciacci, C., Lorusso, L.C., Canonico, B., Falcioni, T., Gallo, G., Canesi, L., 2006. Effects of tumour necrosis factor alpha (TNFLx) on Mytilus haemocytes: role of stress-activated mitogen-activated protein kinases (MAPKs). Biology of the Cell 98, 233-244.
5. Blaise, C., Trottier, S., Gagne, F., Lallement, C., Hansen, P.D., 2002. Immunocompetence of bivalve hemocytes as evaluated by a miniaturized phagocytosis assay. Environmental Toxicology 17, 160-169. (Pubitemid 34784961)
6. Bouchard, B., Gagne, F., Fortier, M., Fournier, M., 2009. An in-situ study of the impacts of urban wastewater on the immune and reproductive systems of the freshwater mussel Elliptio complanata. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 150, 132-140.
7. Bradford, M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248-254.
8. Brousseau, P., Payette, Y., Blakley, B., Boermans, H., Flipo, D., Tryphomonas, H., Fournier, M., 1998. Manual of Immunological Methods. CRP Press, Boston, USA.
9. Canesi, L., Borghi, C., Fabbri, R., Ciacci, C., Lorusso, L.C., Gallo, G., Vergani, L., 2007a. Effects of 17[beta]-estradiol on mussel digestive gland. General and Comparative Endocrinology 153, 40-46. (Pubitemid 47102336)
10. Canesi, L., Ciacci, C., Lorusso, L.C., Betti, M., Gallo, G., Pojana, G., Marcomini, A., 2007b. Effects of Triclosan on Mytilus galloprovincialis hemocyte function and digestive gland enzyme activities: possible modes of action on non target organisms. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 145, 464-472. (Pubitemid 46484489)
11. Canesi, L., Lorusso, L.C., Ciacci, C., Betti, M., Rocchi, M., Pojana, G., Marcomini, A., 2007c. Immunomodulation of Mytilus hemocytes by individual estrogenic chemicals and environmentally relevant mixtures of estrogens: in vitro and in vivo studies. Aquatic Toxicology 81, 36-44. (Pubitemid 46080485)
12. Canesi, L., Gallo, G., Gavioli, M., Pruzzo, C., 2002a. Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microscopy Research and Technique 57, 469-476. (Pubitemid 34701147)
13. Canesi, L., Scarpato, A., Betti, M., Ciacci, C., Pruzzo, C., Gallo, G., 2002b. Bacterial killing by Mytilus hemocyte monolayers as a model for investigating the signaling pathways involved in mussel immune defence. Marine Environmental Research 54, 547-551. (Pubitemid 35286474)
14. Carballal, M.J., Lopez, C., Azevedo, C., Villalba, A., 1997. Enzymes involved in defense functions of hemocytes of mussel Mytilus galloprovincialis. Journal of Invertebrate Pathology 70, 96-105. (Pubitemid 127439465)
15. Chu, F.L.E., Lapeyre, J.F., 1989. Effects of environmental factors and parasitism on hemolymph lysozyme and protein of american oyster (Crassostrea virginica). Journal of Invertebrate Pathology 54, 224-232.
16. Cleuvers, M., 2003. Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicology Letters 142, 185-194. (Pubitemid 36412007)
17. Collen, J., Davison, I.R., 1997. In vivo measurement of active oxygen production in the brown alga Fucus evanescens using 2′,7′- dichlorohydrofluorescein diacetate. Journal of Phycology 33, 643-648. (Pubitemid 27377951)
18. Culic, O., Erakovic, V., Parnham, M.J., 2001. Anti-inflammatory effects of macrolide antibiotics. European Journal of Pharmacology 429, 209-229. (Pubitemid 33043997)
19. Dalhoff, A., 2005. Immunomodulatory activities of fluoroquinolones. Infection 33, 55-70.
20. Dokmeci, D., 2004. Ibuprofen and Alzheimer's disease. Folia Medica 46, 5-10.
21. Dondero, F., Dagnino, A., Jonsson, H., Capri, F., Gastaldi, L., Viarengo, A., 2006. Assessing the occurence of a stress syndrme in mussels (Mytilus edulis) using a combined biomarker/gene expression approach. Aquatic Toxicology 78, s13-s24. (Pubitemid 44294656)
22. Farcy, E., Gagne, F., Martel, L., Fortier, M., Trepanier, S., Brousseau, P., Fournier, M., 2011. Short-term physiological effects of a xenobiotic mixture on the freshwater mussel Elliptio complanata exposed to municipal effluents. Environmental Research 111, 1096-1106.
23. Fatta-Kassinos, D., Meric, S., Nikolaou, A., 2011. Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Analytical and Bioanalytical Chemistry 399, 251-275.
24. Fent, K., Weston, A.A., Caminada, D., 2006. Ecotoxicology of human pharmaceuticals. Aquatic Toxicology 76, 122-159. (Pubitemid 43087657)
25. Fujimoto, Y., Sakuma, S., Inoue, T., Uno, E., Fujita, T., 2002. The endocrine disruptor nonylphenol preferentially blocks cyclooxygenase-1. Life Sciences 70, 2209-2214. (Pubitemid 34251292)
26. Gagné, F., Andre, C., Fortier, M., Fournier, M., 2012. Immunotoxic potential of aeration lagoon effluents for the treatment of domestic wastewaters in the freshwater mussel Elliptio complanata. Journal of Environmental Science 24, 60860-60862. doi:10.1016/S1001-0724(1011).
27. Gagne, F., Blaise, C., Andre, C., 2006a. Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. Ecotoxicology and Environmental Safety 64, 329-336. (Pubitemid 43817169)
28. Gagne, F., Blaise, C., Fournier, M., Hansen, P.D., 2006b. Effects of selected pharmaceutical products on phagocytic activity in Elliptio complanata mussels. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 143, 179-186.
29. Gagne, F., Blaise, C., Aoyama, I., Luo, R., Gagnon, C., Couillard, Y., Campbell, P., Salazar, M., 2002. Biomarker study of a municipal effluent dispersion plume in two species of freshwater mussels. Environmental Toxicology 17, 149-159. (Pubitemid 34784960)
30. Galloway, T.S., Depledge, M.H., 2001. Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10, 5-23. (Pubitemid 32128502)
31. Gourdon, I., Guerin, M.C., Torreilles, J., Roch, P., 2001. Nitric oxide generation by hemocytes of the mussel Mytilus galloprovincialis. Nitric Oxide-Biology and Chemistry 5, 1-6. (Pubitemid 34146166)
32. Hebert, N., Gagne, F., Cejka, P., Cyr, D., Marcogliese, D.J., Blaise, C., Pellerin, J., Fournier, M., 2008. The effects of a primary-treated municipal effluent on the immune system of rainbow trout (Oncorhynchus mykiss): exposure duration and contribution of suspended particles. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology 148, 258-264.
33. Kanoh, S., Rubin, B.K., 2010. Mechanisms of action and clinical application of macrolides as immunomodulatory medications. Clinical Microbiology Reviews 23, 590-603.
34. Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S.D., Barber, L.B., Buxton, H.T., 2002. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a National Reconnaissance. Environmental Science and Technology 36, 1202-1211. (Pubitemid 34228893)
35. Labro, M.T., 2000. Interference of antibacterial agents with phagocyte functions: immunomodulation or "immuno-fairy tales". Clinical Microbiology Reviews 13, 615.
36. Lee, Y.C., Yang, D., 2002. Determination of lysozyme activities in a microplate format. Analytical Biochemistry 310, 223-224. (Pubitemid 35388266)
37. Lhurmann, A., Tholke, J., Behn, I., Schumann, J., Tiegs, G., Hauschildt, S., 1998. Immunomodulating properties of the antibiotic novobiocin in human monocytes. Antimicrobial Agents Chemotherapy 42, 1911-1916. (Pubitemid 28363069)
38. Li, H., Parisi, M.-G., Toubiana, M., Cammarata, M., Roch, P., 2008. Lysozyme gene expression and hemocyte behaviour in the Mediterranean mussel, Mytilus galloprovincialis, after injection of various bacteria or temperature stresses. Fish & Shellfish Immunology 25, 143-152.
39. Menard, L., Escarne, R., Marcogliese, D.J., Cyr, D., Fournier, M., Gagne, F., 2010. The impact of urbqn pollution on the immune system of spottail shiners (Notropis hudsonius) in the St. Lawrence River. Fresenius Environmental Bulletin 19, 1369-1374.
40. Metcalfe, C.D., Koenig, B.G., Bennie, D.T., Servos, M., Ternes, T.A., Hirsch, R., 2003. Occurrence of neutral and acidic drugs in the effluents of Canadian sewage treatment plants. Environmental Toxicology and Chemistry 22, 2872-2880. (Pubitemid 37485216)
41. Mydlarz, L.D., Jones, L.E., Harvell, C.D., 2006. Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annual Review of Ecology Evolution and Systematics, 251-288. (Pubitemid 44907619)
42. Oliver, L.M., Fisher, W.S., Winstead, J.T., Hemmer, B.L., Long, E.R., 2001. Relationships between tissue contaminants and defense-related characteristics of oysters (Crassostrea virginica) from five Florida bays. Aquatic Toxicology 55, 203-222. (Pubitemid 32928480)
43. Ostrovidov, S., Franck, P., Joseph, D., Martarello, L., Kirsch, G., Belleville, F., Nabet, P., Dousset, B., 2000. Screening of new antioxidant molecules using flow cytometry. Journal of Medicinal Chemistry 43, 1762-1769. (Pubitemid 30305009)
44. Pipe, R.K., 1990. Hydrolytic enzymes associated with the antigranulocytes hemocytes of the marine mussel Mytilus edulis. Histochemical Journal 22, 595-603. (Pubitemid 20368329)
45. Pipe, R.K., 1992. Generation of reactive oxygen metabolites by the hemocytes of the mussel Mytilus edulis. Developmental and Comparative Immunology 16, 111-122.
46. Quinn, B., Gagne, F., Blaise, C., 2009. Evaluation of the acute, chronic and teratogenic effects of a mixture of eleven pharmaceuticals on the cnidarian, Hydra attenuata. Science of the Total Environment 407, 1072-1079.
47. Spongberg, A.L., Witter, J.D., 2008. Pharmaceutical compounds in the wastewater process stream in Northwest Ohio. Science of the Total Environment 397, 148-157.
48. Sreenivasan, P.K., Gaffar, A., 2008. Antibacterials as anti-inflammatory agents: dual action agents for oral health. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 93, 227-239. (Pubitemid 351167818)
49. Stefano, G.B., Cadet, P., Mantione, K., Cho, J.J., Jones, D., Zhu, W., 2003. Estrogen signaling at the cell surface coupled to nitric oxide release in Mytilus edulis nervous system. Endocrinology 144, 1234-1240. (Pubitemid 36428464)
50. Tafalla, C., Gomez-Leon, J., Novoa, B., Figueras, A., 2003. Nitric oxide production by carpet shell clam (Ruditapes decussatus) hemocytes. Developmental and Comparative Immunology 27, 197-205. (Pubitemid 36187448)
51. Terzic, S., Senta, I., Ahel, M., Gros, M., Petrovic, M., Barcelo, D., Mueller, J., Knepper, T., Marti, I., Ventura, F., Jovancic, P., Jabucar, D., 2008. Occurrence and fate of emerging wastewater contaminants in Western Balkan Region. Science of the Total Environment 399, 66-77.
52. Verdon, C.P., Burton, B.A., Prior, R.L., 1995. Sample pretreatment with nitrate reductase and glucose-6-phosphate-deshydrogenase quantitatively reduces nitrate while avoiding interference by NADP(+) when the Griess reaction is used to assay for nitrite. Analytical Biochemistry 224, 502-508.
53. Verlicchi, P., Galletti, A., Petrovic, M., Barcelo, D., 2010. Hospital effluents as a source of emerging pollutants: an overview of micropollutants and sustainable treatment options. Journal of Hydrology 389, 416-428.
54. Villamil, L., Gomez-Leon, J., Gomez-Chiarri, M., 2007. Role of nitric oxide in the defenses of Crassostrea virginica to experimental infection with the protozoan parasite Perkinsus marinus. Developmental and Comparative Immunology 31, 968-977. (Pubitemid 47095007)
55. Wheeler, M.A., Smith, S.D., Saito, N., Foster, H.E., Weiss, R.M., 1997. Effect of long-term oral L-arginine on the nitric oxide synthase pathway in the urine from patients with interstitial cystitis. Journal of Urology 158, 2045-2050. (Pubitemid 27481324)
56. Zuccato, E., Castiglioni, S., Fanelli, R., 2005. Identification of the pharmaceuticals for human use contaminating the Italian aquatic environment. Journal of Hazardous Materials 122, 205-209. (Pubitemid 40828486)